Citrus black spot: Difference between revisions

Citrus black spot
Scientific classification
Domain:	Eukaryota
Kingdom:	Fungi
Division:	Ascomycota
Class:	Dothideomycetes
Order:	Botryosphaeriales
Family:	Botryosphaeriaceae
Genus:	Phyllosticta
Species:	P. citricarpa
Binomial name
	Phyllosticta citricarpa; Kiely, (1948)
Synonyms
	Phoma citricarpa McAlpine, (1899); Phoma citricarpa var. mikan Hara; Phyllosticta citricarpa (McAlpine) Aa, (1973); Phyllostictina citricarpa (McAlpine) Petr., (1953);

Citrus black spot
Citrus black spot
	Citrus black spot lesions
Causal agents	Phyllosticta citricarpa
Hosts	Citrus
EPPO Code	GUIGCI

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Citrus black spot is a fungal disease caused by Phyllosticta citricarpa(previously known as Guignardia citricarpa). This Ascomycete fungus affects citrus plants throughout subtropical climates, causing a reduction in both fruit quantity and quality.^{[citation needed]}

Symptoms include both fruit and leaf lesions, the latter being critical to inter-tree dispersal. Strict regulation and management is necessary to control this disease since there are currently not many citrus varieties that are resistant.^{[citation needed]}

Fungus

Phyllosticta citricarpa is a plant pathogen, some strains of which cause a leaf condition called black spot on citrus plants.^[2] As a result, such strains are subject to phytosanitary legislation in the European Union and the United States.^[3]

Metabolite secreted by P. citricarpa have an inhibitory growth effect on some endophytic bacterial species, and stimulatory growth effect on others.^[4]

An isolate of P. citricarpa was found to produce the medically important compound, taxol under certain growth conditions.^[5]

Origin

Citrus Black Spot was first found in Sydney, Australia, in 1895^[6] ^[7] and then appeared in South Africa along the coast of Natal in 1929. It can be found in many countries around the world. These countries include: Argentina, Australia, Brazil, China, Ghana, Mozambique, Philippines, South Africa, Sub-Saharan Africa, Taiwan, The United States and Uruguay. Whether or not Citrus Black Spot is present in Japan and New Zealand is controversial. In both countries the fungus was thought to have been found, but after further testing it was identified as the non-pathogenic strain, Phyllosticta capitalensis, rather than the pathogenic strain Phyllosticta citricarpa which causes Citrus Black Spot.^[8] The disease was first reported in North America during March 2010, in Collier and Hendry counties of southern Florida. The range of the disease in North America has remained limited to Southern Florida at present. Florida has taken measures to try to control this disease, however, it is expected to rapidly spread to other areas over the next few years.^[9]

Hosts

Phyllosticta citricarpa infects citrus plants mostly. However, this fungus is also seen to infect other plants such as golden apple, mango and guava as well.^[10] There are some plants that are more susceptible to the pathogen than others. Lemon and late maturing citrus, such as Valencia orange, are the most susceptible hosts.^{[citation needed]}

Moderately susceptible hosts are Hamlin sweet oranges, tangerine/ mandarin type fruit, and grapefruit.^{[citation needed]}

Though there are some hosts that are more susceptible to Citrus Black Spot than others, any citrus plant that is nutritionally stressed increases its chances of infection.^[11]

Fruit symptoms and signs

Hard spot lesions

Hard spots are the most common lesions. They are small, round, and sunken. The average diameter of hard spot lesions ranges from 3–10 mm (.12-.4 in).^[12]^[13] They have dark red to chocolate brown margins and often have pycnidia in the gray-colored centers.^[14] A green halo may be present around the lesion.^[15]

False melanose lesions

False melanose lesions are characterized by many small, tan, slightly raised lesions. The lesions are much smaller than the hard spot variety with an average diameter of less than 1 mm (.04 in).^[12]^[13] They are found on unripe fruit and are difficult to observe later in the season. Unlike hard spot lesions, no pycnidia are present.^[14]

Cracked spot lesions

These lesions occur on both unripe and ripe fruit. They are large, slightly raised, dark brown spots. Cracked spot lesions do not contain pycnidia. They create raised cracks on the fruit surface that can be difficult to see later in the season.^[14] Studies have suggested a possible interaction between cracked spot lesions and rust mite colonization.^[16]

Freckle spot lesions

Freckle spot lesions are the early form of virulent spot lesions. They are small, reddish, irregularly shaped, and contain many pycnidia.^[13] These lesions are most noticeable during the end of the season, as they are found on mature fruit and during post-harvest storage.^{[citation needed]}

Virulent spot lesions

The mature stage of freckle spot lesions, they are found on mature fruit and during post-harvest storage. They are similar in appearance to the freckle spot lesions, but under high humidity can cover the entire fruit. Because of this direct damage to the fruit, this type of lesion can be economically devastating.^[13]

Leaf symptoms

Leaf symptoms are generally observed on highly susceptible citrus varieties, such as lemons, as well in poorly-managed orchards. The symptoms generally develop from latent infections after the leaves have died. Red-brown, pin-point dots may develop into larger, circular necrotic lesions with gray centers and red or brown margins.^[17]^[18]

Diagnosis

To confirm a diagnosis of Citrus Black Spot, the pathogenic fungus must be isolated in culture. This can be difficult, as culturing of the fruit lesions takes up to 14 days with an efficacy of less than 10%. Diagnosis is also complicated by the morphological similarities of the fungal structures to the non-pathogenic strain Phyllosticta capitalensis (formerly referred to as Guignarida mangiferae).^[19] The two species can be distinguished by molecular testing using PCR.^[20]

Life cycle

After overwintering in leaf debris, ascostroma begin producing ascospores. Ascospore formation is accelerated by sequential wetting and drying of the leaf litter.^[21]^[22] However, very wet conditions inhibit ascospore development due to leaf decomposition and competition from saprophytes.^[23]^[24] The ascospores are ejected from the fruiting bodies of the fungus during rainfall or irrigation and then dispersed by wind and water.^[25] Upon landing on susceptible tissue, the ascospores germinate and form appresoria after a 24-48 hour wetting period.^[26] (Different tissues are susceptible to infection at different times. Leaves are susceptible up to 10 months of age.^[27] Fruits are susceptible during the 4–5 months after fruitset,^[12]^[25] though trees less than ten years old are only susceptible up to 3 months .^[28]) Soon after, the infection peg along with mycelia colonize the area between the cuticle and epidermal wall. The symptoms are not visible right away because the infection remains latent, or dormant, until the fruit is mature.^[12]^[13]

The infection in leaves usually remains latent until the leaves drop, but leaf spots may be found on older leaves.^[21]^[29] The leaf lesions usually produce ascospores, but sometimes produce pycnidia.^[12]^[25]^[30] These pycnidia release pycnidiospores (conidia) in a gelatinous mass.^[31] Under wet conditions, the gelatinous mass dissolves and the spores are dispersed by splashes of water.^[32] This splash-dispersal method limits reinfection to nearby fruit or leaves of the same tree.^[12]^[22] Fruit infections remain latent until fruit maturity. Upon maturing, the mycelium grows into the outer rind, also known as a flavedo. Here in the flavedo, circular lesions form, which are sometimes accompanied by pycnidia. It is important to note that while ascospores can infect fruit, they have not yet been observed developing on fruit.^[21]^[22]^[25]

Management

There is no resistance to Citrus Black Spot and once a tree has been infected there is no known cure causing tree removal to be the best option. Both federal and state governments^[where?] have recommended the following preventative measures. To control Guignardia citriparpa fungicides like copper and/or strobilurins should be applied monthly from early May to the middle of September (in the northern hemisphere). Applications of the fungicides are recommended in early April (northern hemisphere) if that month has experienced more rainfall than usual resulting in the ideal conditions for citrus black spot to form.^{[citation needed]}

Table 1. Recommended Chemical Controls for Citrus Black Spot^[33]

Pesticide	FRAC MOA2	Mature Trees Rate/Acre1
copper fungicide	M1	use label rate
Abound 2.08F3	11	12.4-15.4 fl oz. Do not apply more than 92.3 fl oz/acre/season for all uses. Best applied with petroleum oil.
Gem 25WG3	11	4.0-8.0 oz. Do not apply more than 32 oz/acre/season for all uses.
Gem 500 SC3	11	1.9-3.8 fl oz. Do not apply more than 15.2 fl oz/acre/season for all uses. Best applied with petroleum oil.
Headline3	11	9-12 fl oz. Do not apply more than 54 fl oz/acre/season for all uses. Best applied with petroleum oil.

1)Lower rates can be used on smaller trees. Do not use less than minimum label rate.

2)Mode of action class for citrus pesticides from the Fungicide Resistance Action Committee (FRAC) 20111. Refer to ENY-624, "Pesticide Resistance and Resistance Management," in the 2012 Florida Citrus Pest Management Guide for more details.

3)Do not use more than 4 applications of strobilurin fungicides/season. Do not make more than 2 sequential applications of strobilurin fungicides. ^[34]

Another method of control is to accelerate the leaf litter decomposition under the trees in citrus groves. Accelerating this decomposition reduces the chance for ascospore inoculation which generally takes place in the middle of March. There are three possible methods to hasten this decomposition. One method is to increase the microsprinkler irrigation in the grove to half an hour for at least five days of the week. This form of control should continue for about a month and a half. The second method is to apply urea or ammonium to the leaf litter. The last and final method to accelerate leaf decomposition is to apply lime or calcium carbonate to the litter. Urea, lime, and calcium carbonate reduce the number of fungal structures and spore production.^[35] Since the fungus requires wet conditions to thrive, air flow in the citrus grove should be maximized to reduce leaf wetness.^[18]

Along with these methods it is also important to get rid of debris such as fallen fruit or twigs in a manner that reduces the chances of infecting other plants. Citrus Black Spot can colonize and reproduce on dead twigs. To dispose of citrus debris it should either be heated to a minimum of 180 °F for two hours, incinerated, buried in a landfill, or fed to livestock. Plant trash should be moved with caution if at all to avoid spreading the infectious ascospores. Any trees that are infected with citrus black spot should be removed from the grove and disposed of. These trees must be removed because those that are declining and stressed will often have off season bloom. If there is more than one age of fruit present on the tree, it is possible for the asexual spores on the older fruits to be transferred to young fruits, thereby intensifying the disease. This off season blooming is often more problematic with Valencia oranges when old and new crops overlap; therefore fruits should be harvested before blooming commences.^{[citation needed]}

Importance

Citrus Black Spot has a large economic impact on many countries because the black blemishes make it undesirable for human consumption and therefore the infected fruit cannot be sold. This type of economic impact is felt most in Australia and South Africa where the disease has been present for a number of years.^[36] In Australia, South Africa, and China citrus is of particular importance due to the large role it plays in international trade. A few black spots on as little as one piece of fruit can cause the entire shipment to be rejected. When this happens the shipment usually has to be repackaged and resold to a less sensitive market which leads to large financial losses.^[8] Along with making fruit unsuitable for sale Citrus Black Spot also causes early fruit drop and reduces crop yield.^[11] The reduction in fruit value due to Citrus Black Spot is estimated at 20-30%.^[37]

At the end of 2013, the European Commission announced a ban on most imports of citrus fruit from South Africa because of concerns about the possible transmission of Citrus Black Spot to the EU. This ban was justified by a study by the European Food Safety Authority (EFSA) on the risk of transmission. However, a specially convened panel of eminent scientists from Brazil, Argentina, the USA, Uruguay, Australia and South Africa concluded that there is no risk of transmission through fruit to European climates. It argued that Citrus Black Spot has never spread to new areas with fruit as the cause and citrus fruit has never been shown to be the cause of the spread of the disease. The panel pointed out that it is known to occur only in summer rainfall citrus production areas and that the only way it has been spread to new areas has been through infected propagation material moved to areas where the climate is suitable for its establishment.^[38]

References

^ Wikee, S., Udayanga, D., Crous, P.W., Chukeatirote, E., McKenzie, E.H., Bahkali, A.H., Dai, D. & Hyde, K.D. 2011, "Phyllosticta—an overview of current status of species recognition", Fungal Diversity, vol. 51, no. 1, pp. 43-61
^ "Archived copy" (PDF). Archived from the original (PDF) on 2010-12-02. Retrieved 2014-01-10.{{cite web}}: CS1 maint: archived copy as title (link)
^ Baayen RP, Bonants PJ, Verkley G, et al. (May 2002). "Nonpathogenic Isolates of the Citrus Black Spot Fungus, Guignardia citricarpa, Identified as a Cosmopolitan Endophyte of Woody Plants, P. mangiferae (Phyllosticta capitalensis)". Phytopathology. 92 (5): 464–77. doi:10.1094/PHYTO.2002.92.5.464. PMID 18943020.
^ Araújo WL, Maccheroni W, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, Azevedo JL (March 2001). "Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks". Can. J. Microbiol. 47 (3): 229–36. doi:10.1139/cjm-47-3-229. PMID 11315114. Archived from the original on 2012-12-16.
^ Kumaran RS, Muthumary J, Hur BK (July 2008). "Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica". J. Biosci. Bioeng. 106 (1): 103–6. doi:10.1263/jbb.106.103. PMID 18691540.
^ Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)
^ Citrus Black Spot (Guignardia citricarpa) discovered in Florida, Florida Department of Agriculture and Consumer Services, Division of Plant Industry, https://crec.ifas.ufl.edu/media/crecifasufledu/extension/plant-pathology-/black-spot/citrus-black-spot-pest-alert.pdf, (May 4, 2023)
^ ^a ^b "Archived copy" (PDF). Archived from the original (PDF) on 2018-11-12. Retrieved 2012-10-18.{{cite web}}: CS1 maint: archived copy as title (link)
^ "A manageable disease in the Florida Citrus Industry" (PDF). Edis.ifas.ufl.edu. Retrieved 5 December 2012.
^ "Guignardia citricarpa (citrus black spot)". www.cabi.org. Retrieved 2022-11-05.
^ ^a ^b "USDA APHIS | Plant Pests and Diseases". Aphis.usda.gov.
^ ^a ^b ^c ^d ^e ^f Kotzé, J. M. 2000. Black spot. Pages 23-25 in J. O. Whiteside, S. M. Garnsey, and L. W. Timmer, (eds.). Compendium of Citrus Diseases. American Phytopathological Society, St Paul, MN, USA.
^ ^a ^b ^c ^d ^e "Fact Sheet: Citrus black spot - Citrus Diseases". idtools.org.
^ ^a ^b ^c "UF/IFAS Citrus Extension: Plant Pathology". ufl.edu.
^ Dewdney, Megan; et al. "Citrus Black Spot: Identification, Biology and Control". University of Florida. Archived from the original on 17 February 2013. Retrieved 3 December 2012.
^ EPPO. 2009. Guignardia citricarpa. OEPP/EPPO Bulletin 39:318-327, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Wager, V. A. 1952. The black spot disease of citrus in South Africa. Citrus Grower 227:5-12, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ ^a ^b "Citrus Black Spot". University of Florida. Retrieved 3 December 2012.
^ December 2015, DP 5: Phyllosticta citricarpa (McAlpine) Aa on fruit, International Plant Protection Convention, https://www.fao.org/3/ml511en/ml511en.pdf, (May 4, 2023)
^ "Guignardia citricarpa". EPPO Bulletin. 39 (3): 318–327. 2009. doi:10.1111/j.1365-2338.2009.02319.x.
^ ^a ^b ^c Kiely, T. B. 1948. Preliminary studies on Guignardia citricarpa n. sp.: The ascigerous stage of Phoma citricarpa McAlp. and its relation to black spot of citrus. Proceedings of the Linnaeus Society of New South Wales 73:249-292, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ ^a ^b ^c Kotzé, J. M. 1981. Epidemiology and control of citrus black spot in South Africa. Plant Disease 65:945-950, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Lee, Y. S., and C. S. Huang. 1973. Effect of climatic factors on the development and discharge of ascospores of the citrus black spot fungus. Journal of Taiwan Agriculture Research 22:135-144, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ CABI. 2006. Guignardia citricarpa. Crop Protection Compendium, CD-ROM. CAB International, Commonwealth Agricultural Bureau International (CABI) Wallingford, UK, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ ^a ^b ^c ^d Kotzé, J. M. 1963. Studies on the black spot disease of citrus caused by Guignardia citricarpa Kiely with particular reference to its epiphytology and control at Lebata. Doctoral Thesis, University of Pretoria, Pretoria, South Africa. January, 1963, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)
^ Truter, M., P. M. Labuschagne, J. M. Kotzé, L. Meyer, and L. Korsten. 2007. Failure of Phyllosticta citricarpa pycnidiospores to infect Eureka lemon leaf litter. Australasian Plant Pathology 36:87-93, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Kiely, T. B. 1969. Black spot of citrus. Agricultural Gazette of New South Wales 80(12):658- 662.
^ Whiteside, J. O. 1965. Black spot disease in Rhodesia: A review of current information. Rhodesia Agricultural Journal 64:87-91, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ McOnie, K. C. 1967. Germination and infection of citrus by ascospores of Guignardia citricarpa in relation to control of black spot. Phytopathology 57:743-746, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Korf, H. J. G. 1998. Survival of Phyllosticta citricarpa, anamorph of the citrus black spot pathogen. Master of Science Thesis, University of Pretoria, Pretoria, South Africa. Dec. 1998.
^ Spósito, M. B., L. Amorim, R. B. Bassanezi, A. Bergamin Filho, and B. Hau. 2008. Spatial pattern of black spot incidence within citrus trees related to disease severity and pathogen dispersal. Plant Pathology 57:103-108, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.
^ Communications, IFAS. "St. Lucie County - UF/IFAS Extension" (PDF). stlucie.ifas.ufl.edu. Retrieved 14 July 2018.
^ "FRAC | Error". Archived from the original on 2012-07-23. Retrieved 2012-11-30.
^ Megan M. Dewdney; Timothy S. Schubert; Mark R. Estes; Natalia A. Peres (2016-05-06). "PP279/CG088: 2014 Florida Citrus Pest Management Guide: Citrus Black Spot". ufl.edu.
^ "Guignardia citricarpa | Datasheet | Plantwise". archive.vn. 2013-04-15. Archived from the original on 2013-04-15. Retrieved 2020-04-04.
^ "Citrus black spot" (PDF). Irrec.ifas.ufl.edu. Retrieved 6 March 2022. Reduction fruit value due to CBS: 20 – 30%
^ Agritrade. "Debate on Citrus Black Spot continues". CTA. Archived from the original on 2 October 2014. Retrieved 27 February 2014.

[renamed_from_2_on_20150203132126-1] Wikee, S., Udayanga, D., Crous, P.W., Chukeatirote, E., McKenzie, E.H., Bahkali, A.H., Dai, D. & Hyde, K.D. 2011, "Phyllosticta—an overview of current status of species recognition", Fungal Diversity, vol. 51, no. 1, pp. 43-61

[2] "Archived copy" (PDF). Archived from the original (PDF) on 2010-12-02. Retrieved 2014-01-10.{{cite web}}: CS1 maint: archived copy as title (link)

[pmid18943020-3] Baayen RP, Bonants PJ, Verkley G, et al. (May 2002). "Nonpathogenic Isolates of the Citrus Black Spot Fungus, Guignardia citricarpa, Identified as a Cosmopolitan Endophyte of Woody Plants, P. mangiferae (Phyllosticta capitalensis)". Phytopathology. 92 (5): 464–77. doi:10.1094/PHYTO.2002.92.5.464. PMID 18943020.

[pmid11315114-4] Araújo WL, Maccheroni W, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, Azevedo JL (March 2001). "Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks". Can. J. Microbiol. 47 (3): 229–36. doi:10.1139/cjm-47-3-229. PMID 11315114. Archived from the original on 2012-12-16.

[pmid18691540-5] Kumaran RS, Muthumary J, Hur BK (July 2008). "Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica". J. Biosci. Bioeng. 106 (1): 103–6. doi:10.1263/jbb.106.103. PMID 18691540.

[6] Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)

[7] Citrus Black Spot (Guignardia citricarpa) discovered in Florida, Florida Department of Agriculture and Consumer Services, Division of Plant Industry, https://crec.ifas.ufl.edu/media/crecifasufledu/extension/plant-pathology-/black-spot/citrus-black-spot-pest-alert.pdf, (May 4, 2023)

[dissertation-8] "Archived copy" (PDF). Archived from the original (PDF) on 2018-11-12. Retrieved 2012-10-18.{{cite web}}: CS1 maint: archived copy as title (link)

[9] "A manageable disease in the Florida Citrus Industry" (PDF). Edis.ifas.ufl.edu. Retrieved 5 December 2012.

[10] "Guignardia citricarpa (citrus black spot)". www.cabi.org. Retrieved 2022-11-05.

[aphis-11] "USDA APHIS | Plant Pests and Diseases". Aphis.usda.gov.

[Kotze_2000-12] ^ ^a ^b ^c ^d ^e ^f Kotzé, J. M. 2000. Black spot. Pages 23-25 in J. O. Whiteside, S. M. Garnsey, and L. W. Timmer, (eds.). Compendium of Citrus Diseases. American Phytopathological Society, St Paul, MN, USA.

[idtools.org-13] "Fact Sheet: Citrus black spot - Citrus Diseases". idtools.org.

[UF_extension_CBS-14] "UF/IFAS Citrus Extension: Plant Pathology". ufl.edu.

[15] Dewdney, Megan; et al. "Citrus Black Spot: Identification, Biology and Control". University of Florida. Archived from the original on 17 February 2013. Retrieved 3 December 2012.

[16] EPPO. 2009. Guignardia citricarpa. OEPP/EPPO Bulletin 39:318-327, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[17] Wager, V. A. 1952. The black spot disease of citrus in South Africa. Citrus Grower 227:5-12, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[Citrus_Black_Spot-18] "Citrus Black Spot". University of Florida. Retrieved 3 December 2012.

[19] December 2015, DP 5: Phyllosticta citricarpa (McAlpine) Aa on fruit, International Plant Protection Convention, https://www.fao.org/3/ml511en/ml511en.pdf, (May 4, 2023)

[20] "Guignardia citricarpa". EPPO Bulletin. 39 (3): 318–327. 2009. doi:10.1111/j.1365-2338.2009.02319.x.

[Kiely_1948-21] Kiely, T. B. 1948. Preliminary studies on Guignardia citricarpa n. sp.: The ascigerous stage of Phoma citricarpa McAlp. and its relation to black spot of citrus. Proceedings of the Linnaeus Society of New South Wales 73:249-292, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[Kotze_1981-22] Kotzé, J. M. 1981. Epidemiology and control of citrus black spot in South Africa. Plant Disease 65:945-950, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[23] Lee, Y. S., and C. S. Huang. 1973. Effect of climatic factors on the development and discharge of ascospores of the citrus black spot fungus. Journal of Taiwan Agriculture Research 22:135-144, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[24] CABI. 2006. Guignardia citricarpa. Crop Protection Compendium, CD-ROM. CAB International, Commonwealth Agricultural Bureau International (CABI) Wallingford, UK, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[Kotze_1963-25] Kotzé, J. M. 1963. Studies on the black spot disease of citrus caused by Guignardia citricarpa Kiely with particular reference to its epiphytology and control at Lebata. Doctoral Thesis, University of Pretoria, Pretoria, South Africa. January, 1963, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[26] Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)

[27] Truter, M., P. M. Labuschagne, J. M. Kotzé, L. Meyer, and L. Korsten. 2007. Failure of Phyllosticta citricarpa pycnidiospores to infect Eureka lemon leaf litter. Australasian Plant Pathology 36:87-93, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[28] Kiely, T. B. 1969. Black spot of citrus. Agricultural Gazette of New South Wales 80(12):658- 662.

[29] Whiteside, J. O. 1965. Black spot disease in Rhodesia: A review of current information. Rhodesia Agricultural Journal 64:87-91, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[30] McOnie, K. C. 1967. Germination and infection of citrus by ascospores of Guignardia citricarpa in relation to control of black spot. Phytopathology 57:743-746, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[31] Korf, H. J. G. 1998. Survival of Phyllosticta citricarpa, anamorph of the citrus black spot pathogen. Master of Science Thesis, University of Pretoria, Pretoria, South Africa. Dec. 1998.

[32] Spósito, M. B., L. Amorim, R. B. Bassanezi, A. Bergamin Filho, and B. Hau. 2008. Spatial pattern of black spot incidence within citrus trees related to disease severity and pathogen dispersal. Plant Pathology 57:103-108, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease. 2010.

[33] Communications, IFAS. "St. Lucie County - UF/IFAS Extension" (PDF). stlucie.ifas.ufl.edu. Retrieved 14 July 2018.

[34] "FRAC | Error". Archived from the original on 2012-07-23. Retrieved 2012-11-30.

[35] Megan M. Dewdney; Timothy S. Schubert; Mark R. Estes; Natalia A. Peres (2016-05-06). "PP279/CG088: 2014 Florida Citrus Pest Management Guide: Citrus Black Spot". ufl.edu.

[36] "Guignardia citricarpa | Datasheet | Plantwise". archive.vn. 2013-04-15. Archived from the original on 2013-04-15. Retrieved 2020-04-04.

[37] "Citrus black spot" (PDF). Irrec.ifas.ufl.edu. Retrieved 6 March 2022. Reduction fruit value due to CBS: 20 – 30%

[38] Agritrade. "Debate on Citrus Black Spot continues". CTA. Archived from the original on 2 October 2014. Retrieved 27 February 2014.

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+{{short description|Fungal disease that affects citrus fruit}}
 {{Infobox plant disease
 | name            = Citrus black spot
 | image           = Citrus Black Spot lesions.jpg
 | caption         = Citrus black spot lesions
 | common_names    =
 | causal_agents   = ''Phyllosticta citricarpa''<ref name=renamed_from_2_on_20150203132126>Wikee, S., Udayanga, D., Crous, P.W., Chukeatirote, E., McKenzie, E.H., Bahkali, A.H., Dai, D. & Hyde, K.D. 2011, "Phyllosticta—an overview of current status of species recognition", Fungal Diversity, vol. 51, no. 1, pp. 43-61</ref>
 | hosts           = Citrus
 | vectors         =
 | EPPO_codes      = GUIGCI
 | distribution    =
 }}
-'''Citrus black spot''' is a fungal disease caused by '''''Guignardia citricarpa'''''. This [[Ascomycete]] fungus affects citrus plants throughout subtropical climates, causing a reduction in both fruit quantity and quality. Symptoms include both fruit and leaf lesions, the latter being critical to inter-tree dispersal. Strict regulation and management is necessary to control this disease since there are currently no citrus varieties that are resistant.
+'''Citrus black spot''' is a fungal disease caused by '''''[https://www.cabi.org/isc/datasheet/26154 Phyllosticta citricarpa]'''''(previously known as ''Guignardia citricarpa)''. This [[Ascomycete]] fungus affects citrus plants throughout subtropical climates, causing a reduction in both fruit quantity and quality.{{cn|date=November 2022}}
+Symptoms include both fruit and leaf lesions, the latter being critical to inter-tree dispersal. Strict regulation and management is necessary to control this disease since there are currently not many citrus varieties that are resistant.{{cn|date=November 2022}}
-{{Taxobox
-| name = ''Guignardia citricarpa''
+{{Speciesbox
-| regnum = [[Fungi]]
+| image =
-| phylum = [[Ascomycota]]
+| genus = Phyllosticta
-| classis = [[Dothideomycetes]]
+| species = citricarpa
-| subclassis = [[Incertae sedis]]
+| authority = Kiely, (1948)
-| ordo = [[Botryosphaeriales]]
+| synonyms =
-| familia = [[Botryosphaeriaceae]]
+* ''Phoma citricarpa'' <small>McAlpine, (1899)</small>
-| genus = ''[[Guignardia]]''
+* ''Phoma citricarpa var. mikan'' <small>Hara</small>
-| species = '''''G. citricarpa'''''
-| binomial = ''Guignardia citricarpa''
+* ''Phyllosticta citricarpa'' <small>(McAlpine) Aa, (1973)</small>
+* ''Phyllostictina citricarpa'' <small>(McAlpine) Petr., (1953)</small>
-| binomial_authority = Kiely, (1948)
-| synonyms =
-*''Phoma citricarpa'' <small>McAlpine, (1899)</small>
-*''Phoma citricarpa var. mikan'' <small>Hara</small>
-*''Phyllosticta citricarpa'' <small>(McAlpine) Aa, (1973)</small>
-*''Phyllostictina citricarpa'' <small>(McAlpine) Petr., (1953)</small>
 }}
 ==Fungus==
-''Guignardia citricarpa'' is a [[Plant pathology|plant pathogen]], some strains of which cause a [[leaf]] condition called ''black spot'' on [[citrus]] plants.<ref>{{Cite web |url=http://www.doacs.state.fl.us/pi/pest_alerts/pdf/citrus-black-spot-pest-alert.pdf |title=Archived copy |access-date=2014-01-10 |archive-url=https://web.archive.org/web/20101202072828/http://www.doacs.state.fl.us/pi/pest_alerts/pdf/citrus-black-spot-pest-alert.pdf |archive-date=2010-12-02 |url-status=dead }}</ref>  As a result, such strains are subject to phytosanitary legislation in the [[European Union]] and the [[United States]].<ref name="pmid18943020">{{cite journal  |vauthors=Baayen RP, Bonants PJ, Verkley G, etal |title=Nonpathogenic Isolates of the Citrus Black Spot Fungus, Guignardia citricarpa, Identified as a Cosmopolitan Endophyte of Woody Plants, G. mangiferae (Phyllosticta capitalensis) |journal=Phytopathology |volume=92 |issue=5 |pages=464–77 |date=May 2002 |pmid=18943020 |doi=10.1094/PHYTO.2002.92.5.464 |url=}}</ref>
+''Phyllosticta citricarpa'' is a [[Plant pathology|plant pathogen]], some strains of which cause a [[leaf]] condition called ''black spot'' on [[citrus]] plants.<ref>{{Cite web |url=http://www.doacs.state.fl.us/pi/pest_alerts/pdf/citrus-black-spot-pest-alert.pdf |title=Archived copy |access-date=2014-01-10 |archive-url=https://web.archive.org/web/20101202072828/http://www.doacs.state.fl.us/pi/pest_alerts/pdf/citrus-black-spot-pest-alert.pdf |archive-date=2010-12-02 |url-status=dead }}</ref>  As a result, such strains are subject to phytosanitary legislation in the [[European Union]] and the [[United States]].<ref name="pmid18943020">{{cite journal  |vauthors=Baayen RP, Bonants PJ, Verkley G, etal |title=Nonpathogenic Isolates of the Citrus Black Spot Fungus, Guignardia citricarpa, Identified as a Cosmopolitan Endophyte of Woody Plants, P. mangiferae (Phyllosticta capitalensis) |journal=Phytopathology |volume=92 |issue=5 |pages=464–77 |date=May 2002 |pmid=18943020 |doi=10.1094/PHYTO.2002.92.5.464 |doi-access= }}</ref>
-[[Metabolite]] secreted by ''G. citricarpa'' have an inhibitory growth effect on some [[endophytic]] bacterial species, and stimulatory growth effect on others.<ref name="pmid11315114">{{cite journal |vauthors=Araújo WL, Maccheroni W, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, Azevedo JL |title=Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks |journal=Can. J. Microbiol. |volume=47 |issue=3 |pages=229–36 |date=March 2001 |pmid=11315114 |doi= 10.1139/cjm-47-3-229|url=http://article.pubs.nrc-cnrc.gc.ca/ppv/RPViewDoc?issn=0008-4166&volume=47&issue=3&startPage=229}}</ref>
+[[Metabolite]] secreted by ''P. citricarpa'' have an inhibitory growth effect on some [[endophytic]] bacterial species, and stimulatory growth effect on others.<ref name="pmid11315114">{{cite journal |vauthors=Araújo WL, Maccheroni W, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, Azevedo JL |title=Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks |journal=Can. J. Microbiol. |volume=47 |issue=3 |pages=229–36 |date=March 2001 |pmid=11315114 |doi=10.1139/cjm-47-3-229 |url=http://article.pubs.nrc-cnrc.gc.ca/ppv/RPViewDoc?issn=0008-4166&volume=47&issue=3&startPage=229 |archive-url=https://archive.today/20121216041513/http://article.pubs.nrc-cnrc.gc.ca/ppv/RPViewDoc?issn=0008-4166&volume=47&issue=3&startPage=229 |url-status=dead |archive-date=2012-12-16 }}</ref>
-An isolate of ''G. citricarpa'' was found to produce the medically important compound, [[taxol]] under certain growth conditions.<ref name="pmid18691540">{{cite journal |vauthors=Kumaran RS, Muthumary J, Hur BK |title=Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica |journal=J. Biosci. Bioeng. |volume=106 |issue=1 |pages=103–6 |date=July 2008 |pmid=18691540 |doi=10.1263/jbb.106.103 |url=}}</ref>
+An isolate of ''P. citricarpa'' was found to produce the medically important compound, [[taxol]] under certain growth conditions.<ref name="pmid18691540">{{cite journal |vauthors=Kumaran RS, Muthumary J, Hur BK |title=Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica |journal=J. Biosci. Bioeng. |volume=106 |issue=1 |pages=103–6 |date=July 2008 |pmid=18691540 |doi=10.1263/jbb.106.103 }}</ref>
 ==Origin==
+Citrus Black Spot was first found in [[Sydney|Sydney, Australia]], in 1895<ref>Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)
-Citrus Black Spot was first found in [[Sydney|Sydney, Australia]], in 1879 and then appeared in South Africa along the coast of [[Natal Province|Natal]] in 1929. It can be found in many countries around the world. These countries include: Argentina, Australia, Brazil, China, Ghana, Mozambique, Philippines, South Africa, Sub-Saharan Africa, Taiwan, The United States and Uruguay. Whether or not Citrus Black Spot is present in Japan and New Zealand is controversial. In both countries the fungus was thought to have been found, but after further testing it was identified as the [[Pathogenic_fungus|non-pathogenic strain]], ''Guignardia mangiferae'', rather than the pathogenic strain ''Guignardia citricarpa'' which causes Citrus Black Spot.<ref name=dissertation>[http://upetd.up.ac.za/thesis/available/etd-11192008-091812/unrestricted/dissertation.pdf]</ref> This disease is relatively new to North America; it was first seen in Southern Florida March, 2010. Though Florida has taken measures to try to control this disease it is expected to rapidly spread to other areas over the next few years.<ref>{{cite web|title=A manageable disease in the Florida Citrus Industry|url=http://edis.ifas.ufl.edu/pdffiles/PP/PP28100.pdf|accessdate=5 December 2012}}</ref>
+</ref> <ref>Citrus Black Spot (Guignardia citricarpa) discovered in Florida, Florida Department of Agriculture and Consumer Services, Division of Plant Industry, https://crec.ifas.ufl.edu/media/crecifasufledu/extension/plant-pathology-/black-spot/citrus-black-spot-pest-alert.pdf, (May 4, 2023)</ref> and then appeared in South Africa along the coast of [[Natal Province|Natal]] in 1929. It can be found in many countries around the world. These countries include: Argentina, Australia, Brazil, China, Ghana, Mozambique, Philippines, South Africa, Sub-Saharan Africa, Taiwan, The United States and Uruguay. Whether or not Citrus Black Spot is present in Japan and New Zealand is controversial. In both countries the fungus was thought to have been found, but after further testing it was identified as the [[Pathogenic fungus|non-pathogenic strain]], ''Phyllosticta  capitalensis'', rather than the pathogenic strain ''Phyllosticta citricarpa'' which causes Citrus Black Spot.<ref name=dissertation>{{Cite web |url=http://upetd.up.ac.za/thesis/available/etd-11192008-091812/unrestricted/dissertation.pdf |title=Archived copy |access-date=2012-10-18 |archive-date=2018-11-12 |archive-url=https://web.archive.org/web/20181112141542/http://upetd.up.ac.za/thesis/available/etd-11192008-091812/unrestricted/dissertation.pdf |url-status=dead }}</ref> The disease was first reported in North America during March 2010, in Collier and Hendry counties of southern Florida. The range of the disease in North America has remained limited to Southern Florida at present. Florida has taken measures to try to control this disease, however, it is expected to rapidly spread to other areas over the next few years.<ref>{{cite web|title=A manageable disease in the Florida Citrus Industry|url=http://edis.ifas.ufl.edu/pdffiles/PP/PP28100.pdf|format=PDF|website=Edis.ifas.ufl.edu|access-date=5 December 2012}}</ref>
 ==Hosts==
+''Phyllosticta citricarpa'' infects [[citrus]] plants mostly. However, this fungus is also seen to infect other plants such as golden apple, mango and guava as well.<ref>{{Cite web |title=Guignardia citricarpa (citrus black spot) |url=https://www.cabi.org/isc/datasheet/26154 |access-date=2022-11-05 |website=www.cabi.org |language=en}}</ref> There are some plants that are more susceptible to the pathogen than others. [[Lemon]] and late maturing citrus, such as [[Valencia orange]], are the most susceptible hosts.{{cn|date=November 2022}}
-''Guignardia citricarpa'' will infect all types of [[citrus]] plants; however, there are some plants that are more susceptible to the pathogen than others. [[Lemon]] and late maturing citrus such as [[Valencia orange]] are the most susceptible hosts. Moderately susceptible hosts are Hamlin sweet oranges, tangerine/ mandarin type fruit, and [[grapefruit]]. Though there are some hosts that are more susceptible to Citrus Black Spot than others, any citrus plant that is nutritionally stressed increases its chances of infection.<ref name=aphis>{{cite web | url=http://www.aphis.usda.gov/plant_health/plant_pest_info/citrus/black_spot.shtml | title=USDA APHIS &#124; Plant Pests and Diseases}}</ref>
+Moderately susceptible hosts are Hamlin sweet oranges, tangerine/ mandarin type fruit, and [[grapefruit]].{{cn|date=November 2022}}
-==Fruit Symptoms and Signs==
+Though there are some hosts that are more susceptible to Citrus Black Spot than others, any citrus plant that is nutritionally stressed increases its chances of infection.<ref name="aphis">{{cite web | url=http://www.aphis.usda.gov/plant_health/plant_pest_info/citrus/black_spot.shtml | title=USDA APHIS {{pipe}} Plant Pests and Diseases|website=Aphis.usda.gov}}</ref>
-===Hard Spot Lesions===
+==Fruit symptoms and signs==
+===Hard spot lesions===
 [[File:Citrus Black Spot.jpg|thumb|left|Hard spot lesions on an orange host]]
 Hard spots are the most common lesions. They are small, round, and sunken. The average diameter of hard spot lesions ranges from 3–10&nbsp;mm (.12-.4 in).<ref name="Kotze 2000" /><ref name="idtools.org">{{cite web|url=http://idtools.org/id/citrus/diseases/factsheet.php?name=Citrus%20black%20spot|title=Fact Sheet: Citrus black spot - Citrus Diseases|work=idtools.org}}</ref>
-They have dark red to chocolate brown margins and often have pycnidia in the gray-colored centers.<ref name="UF extension CBS">{{cite web|url=http://www.crec.ifas.ufl.edu/extension/black_spot/citrus_black_spot.shtml|title=UF/IFAS Citrus Extension: Plant Pathology|work=ufl.edu}}</ref> A green halo may be present around the lesion.<ref>{{cite web|last=Dewdney|first=Megan|title=Citrus Black Spot: Identification, Biology and Control|url=http://www.crec.ifas.ufl.edu/extension/greening/misc/index010.shtml|publisher=University of Florida|accessdate=3 December 2012|display-authors=etal}}</ref>
+They have dark red to chocolate brown margins and often have pycnidia in the gray-colored centers.<ref name="UF extension CBS">{{cite web|url=http://www.crec.ifas.ufl.edu/extension/black_spot/citrus_black_spot.shtml|title=UF/IFAS Citrus Extension: Plant Pathology|work=ufl.edu}}</ref> A green halo may be present around the lesion.<ref>{{cite web|last=Dewdney|first=Megan|title=Citrus Black Spot: Identification, Biology and Control|url=http://www.crec.ifas.ufl.edu/extension/greening/misc/index010.shtml|publisher=University of Florida|access-date=3 December 2012|display-authors=etal|archive-url=https://web.archive.org/web/20130217081948/http://www.crec.ifas.ufl.edu/extension/greening/misc/index010.shtml|archive-date=17 February 2013|url-status=dead}}</ref>
-===False Melanose Lesions===
+===False melanose lesions===
 False melanose lesions are characterized by many small, tan, slightly raised lesions. The lesions are much smaller than the hard spot variety with an average diameter of less than 1&nbsp;mm (.04 in).<ref name="Kotze 2000" /><ref name="idtools.org"/>
 They are found on unripe fruit and are difficult to observe later in the season. Unlike hard spot lesions, no pycnidia are present.<ref name="UF extension CBS" />
-===Cracked Spot Lesions===
+===Cracked spot lesions===
 [[File:Citrus Black Spot on Valencia orange.jpg|thumb|Cracked spot lesions on a Valencia orange]]
 These lesions occur on both unripe and ripe fruit. They are large, slightly raised, dark brown spots. Cracked spot lesions do not contain pycnidia. They create raised cracks on the fruit surface that can be difficult to see later in the season.<ref name="UF extension CBS" /> Studies have suggested a possible interaction between cracked spot lesions and rust mite colonization.<ref>EPPO. 2009. Guignardia citricarpa. OEPP/EPPO Bulletin 39:318-327, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref>
-===Freckle Spot Lesions===
+===Freckle spot lesions===
-Freckle spot lesions are the early form of virulent spot lesions. They are small, reddish, irregularly shaped, and contain many pycnidia.<ref name="idtools.org"/> These lesions are most noticeable during the end of the season, as they are found on mature fruit and during post-harvest storage.
+Freckle spot lesions are the early form of virulent spot lesions. They are small, reddish, irregularly shaped, and contain many pycnidia.<ref name="idtools.org"/> These lesions are most noticeable during the end of the season, as they are found on mature fruit and during post-harvest storage.{{cn|date=November 2022}}
-===Virulent Spot Lesions===
+===Virulent spot lesions===
 The mature stage of freckle spot lesions, they are found on mature fruit and during post-harvest storage. They are similar in appearance to the freckle spot lesions, but under high humidity can cover the entire fruit. Because of this direct damage to the fruit, this type of lesion can be economically devastating.<ref name="idtools.org"/>
-==Leaf Symptoms==
+==Leaf symptoms==
-Leaf symptoms are only noticeable on highly susceptible citrus plants; lemons in particular. The symptoms generally develop from latent infections after the leaves have died. Red-brown, pin-point dots may develop into larger, circular necrotic lesions with gray centers and red or brown margins.<ref>Wager, V. A. 1952. The black spot disease of citrus in South Africa. Citrus Grower 227:5-12, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref name="Citrus Black Spot">{{cite web|title=Citrus Black Spot|url=http://www.crec.ifas.ufl.edu/extension/black_spot/citrus_black_spot.shtml|publisher=University of Florida|accessdate=3 December 2012}}</ref>
+Leaf symptoms are generally observed on highly susceptible citrus varieties, such as lemons, as well in poorly-managed orchards. The symptoms generally develop from latent infections after the leaves have died. Red-brown, pin-point dots may develop into larger, circular necrotic lesions with gray centers and red or brown margins.<ref>Wager, V. A. 1952. The black spot disease of citrus in South Africa. Citrus Grower 227:5-12, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref name="Citrus Black Spot">{{cite web|title=Citrus Black Spot|url=http://www.crec.ifas.ufl.edu/extension/black_spot/citrus_black_spot.shtml|publisher=University of Florida|access-date=3 December 2012}}</ref>
 ==Diagnosis==
-To confirm a diagnosis of Citrus Black Spot, the pathogenic fungus must be isolated in culture. This can be difficult, as culturing of the fruit lesions takes up to 14 days with an efficacy of less than 10%. Diagnosis is also complicated by the morphological similarities of the fungal structures to the non-pathogenic strain ''Guignarida mangiferae''. The two species can be distinguished by molecular testing using [[PCR]].<ref>{{Cite journal|title=Guignardia citricarpa|journal=EPPO Bulletin|volume=39|issue=3|pages=318–327|doi=10.1111/j.1365-2338.2009.02319.x|year=2009}}</ref>
+To confirm a diagnosis of Citrus Black Spot, the pathogenic fungus must be isolated in culture. This can be difficult, as culturing of the fruit lesions takes up to 14 days with an efficacy of less than 10%. Diagnosis is also complicated by the morphological similarities of the fungal structures to the non-pathogenic strain ''Phyllosticta capitalensis'' (formerly referred to as ''Guignarida mangiferae'').<ref>December 2015, DP 5: Phyllosticta citricarpa (McAlpine) Aa on fruit, International Plant Protection Convention, https://www.fao.org/3/ml511en/ml511en.pdf, (May 4, 2023)</ref> The two species can be distinguished by molecular testing using [[Polymerase chain reaction|PCR]].<ref>{{Cite journal|title=Guignardia citricarpa|journal=EPPO Bulletin|volume=39|issue=3|pages=318–327|doi=10.1111/j.1365-2338.2009.02319.x|year=2009|doi-access=}}</ref>
-==Life Cycle==
+==Life cycle==
-After overwintering in leaf debris, ascostroma begin producing [[ascospores]]. Ascospore formation is accelerated by sequential wetting and drying of the leaf litter.<ref name="Kiely 1948">Kiely, T. B. 1948. Preliminary studies on Guignardia citricarpa n. sp.: The ascigerous stage of Phoma citricarpa McAlp. and its relation to black spot of citrus. Proceedings of the Linnaeus Society of New South Wales 73:249-292, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref name="Kotze 1981">Kotzé, J. M. 1981. Epidemiology and control of citrus black spot in South Africa. Plant Disease 65:945-950, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> However, very wet conditions inhibit ascospore development due to leaf decomposition and competition from saprophytes.<ref>Lee, Y. S., and C. S. Huang. 1973. Effect of climatic factors on the development and discharge of ascospores of the citrus black spot fungus. Journal of Taiwan Agriculture Research 22:135-144, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref>CABI. 2006. Guignardia citricarpa. Crop Protection Compendium, CD-ROM. CAB International, Commonwealth Agricultural Bureau International (CABI) Wallingford, UK, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> The ascospores are ejected from the fruiting bodies of the fungus during rainfall or irrigation and then dispersed by wind and water.<ref name="Kotze 1963">Kotzé, J. M. 1963. Studies on the black spot disease of citrus caused by Guignardia citricarpa Kiely with particular reference to its epiphytology and control at Lebata. Doctoral Thesis, University of Pretoria, Pretoria, South Africa. January, 1963, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> Upon landing on susceptible tissue, the ascospores germinate and form [[appresoria]]. (Different tissues are susceptible to infection at different times. Leaves are susceptible up to 10 months of age.<ref>Truter, M., P. M. Labuschagne, J. M. Kotzé, L. Meyer, and L. Korsten. 2007. Failure of Phyllosticta citricarpa [[pycnidiospore]]s to infect Eureka lemon leaf litter. Australasian Plant Pathology 36:87-93, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> Fruits are susceptible during the 4–5 months after fruitset,<ref name="Kotze 2000">Kotzé, J. M. 2000. Black spot. Pages 23-25 in J. O. Whiteside, S. M. Garnsey, and L. W. Timmer, (eds.). Compendium of Citrus Diseases. American Phytopathological Society, St Paul, MN, USA.</ref><ref name="Kotze 1963" /> though trees less than ten years old are only susceptible up to 3 months .<ref>Kiely, T. B. 1969. Black spot of citrus. Agricultural Gazette of New South Wales 80(12):658-
+After overwintering in leaf debris, ascostroma begin producing [[ascospores]]. Ascospore formation is accelerated by sequential wetting and drying of the [[leaf litter]].<ref name="Kiely 1948">Kiely, T. B. 1948. Preliminary studies on Guignardia citricarpa n. sp.: The ascigerous stage of Phoma citricarpa McAlp. and its relation to black spot of citrus. Proceedings of the Linnaeus Society of New South Wales 73:249-292, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref name="Kotze 1981">Kotzé, J. M. 1981. Epidemiology and control of citrus black spot in South Africa. Plant Disease 65:945-950, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> However, very wet conditions inhibit ascospore development due to leaf decomposition and competition from saprophytes.<ref>Lee, Y. S., and C. S. Huang. 1973. Effect of climatic factors on the development and discharge of ascospores of the citrus black spot fungus. Journal of Taiwan Agriculture Research 22:135-144, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref><ref>CABI. 2006. Guignardia citricarpa. Crop Protection Compendium, CD-ROM. CAB International, Commonwealth Agricultural Bureau International (CABI) Wallingford, UK, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> The ascospores are ejected from the fruiting bodies of the fungus during rainfall or irrigation and then dispersed by wind and water.<ref name="Kotze 1963">Kotzé, J. M. 1963. Studies on the black spot disease of citrus caused by Guignardia citricarpa Kiely with particular reference to its epiphytology and control at Lebata. Doctoral Thesis, University of Pretoria, Pretoria, South Africa. January, 1963, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> Upon landing on susceptible tissue, the ascospores germinate and form [[appresoria]] after a 24-48 hour wetting period.<ref>Citrus Black Spot Pest Profile, California Department of Food and Agriculture, https://www.cdfa.ca.gov/citrus/pests_diseases/cbs.html, (May 4, 2023)
+</ref> (Different tissues are susceptible to infection at different times. Leaves are susceptible up to 10 months of age.<ref>Truter, M., P. M. Labuschagne, J. M. Kotzé, L. Meyer, and L. Korsten. 2007. Failure of Phyllosticta citricarpa [[pycnidiospore]]s to infect Eureka lemon leaf litter. Australasian Plant Pathology 36:87-93, cited in Tara Holtz USDA-APHIS-PPQ-CPHST-PERAL ''Risk assessment of Citrus spp. fruit as a pathway for the introduction of Guignardia citricarpa Kiely, the organism that causes Citrus Black Spot disease''. 2010.</ref> Fruits are susceptible during the 4–5 months after fruitset,<ref name="Kotze 2000">Kotzé, J. M. 2000. Black spot. Pages 23-25 in J. O. Whiteside, S. M. Garnsey, and L. W. Timmer, (eds.). Compendium of Citrus Diseases. American Phytopathological Society, St Paul, MN, USA.</ref><ref name="Kotze 1963" /> though trees less than ten years old are only susceptible up to 3 months .<ref>Kiely, T. B. 1969. Black spot of citrus. Agricultural Gazette of New South Wales 80(12):658-
 .</ref>) Soon after, the infection peg along with mycelia colonize the area between the cuticle and epidermal wall. The symptoms are not visible right away because the infection remains latent, or dormant, until the fruit is mature.<ref name="Kotze 2000" /><ref name="idtools.org"/>
@@ Line 79: / Line 80: @@
 ==Management==
-There is no resistance to Citrus Black Spot and once a tree has been infected there is no known cure causing tree removal to be the best option. Both federal and state governments have recommended the following preventative measures.
+There is no resistance to Citrus Black Spot and once a tree has been infected there is no known cure causing tree removal to be the best option. Both federal and state governments{{Where|date=February 2020}} have recommended the following preventative measures.
-To control ''Guignardia citriparpa'' fungicides like copper and/or strobilurins should be applied monthly from early May to the middle of September (in the northern hemisphere).  Applications of the fungicides are recommended in early April (northern hemisphere) if that month has experienced more rainfall than usual resulting in the ideal conditions for citrus black spot to form.
+To control ''Guignardia citriparpa'' fungicides like copper and/or strobilurins should be applied monthly from early May to the middle of September (in the northern hemisphere).  Applications of the fungicides are recommended in early April (northern hemisphere) if that month has experienced more rainfall than usual resulting in the ideal conditions for citrus black spot to form.{{cn|date=November 2022}}
-Table 1. Recommended Chemical Controls for Citrus Black Spot<ref>{{cite web|url=http://stlucie.ifas.ufl.edu/documents/CBSManagementTimingScheduleCompatibilityMode.pdf|title=St. Lucie County - UF/IFAS Extension|first=IFAS|last=Communications|date=|website=stlucie.ifas.ufl.edu|accessdate=14 July 2018}}</ref>
+Table 1. Recommended Chemical Controls for Citrus Black Spot<ref>{{cite web|url=http://stlucie.ifas.ufl.edu/documents/CBSManagementTimingScheduleCompatibilityMode.pdf|title=St. Lucie County - UF/IFAS Extension|first=IFAS|last=Communications|website=stlucie.ifas.ufl.edu|access-date=14 July 2018}}</ref>
 {|border="1" cellpadding="5"
 |-
@@ Line 114: / Line 115: @@
 )Do not use more than 4 applications of strobilurin fungicides/season. Do not make more than 2 sequential applications of strobilurin fungicides.
-<ref>{{cite web|url=http://www.frac.info/frac/index.htm |title=FRAC &#124; Error |accessdate=2012-11-30 |url-status=dead |archiveurl=https://web.archive.org/web/20120723052103/http://www.frac.info/frac/index.htm |archivedate=2012-07-23 }}</ref>
+<ref>{{cite web|url=http://www.frac.info/frac/index.htm |title=FRAC {{pipe}} Error |access-date=2012-11-30 |url-status=dead |archive-url=https://web.archive.org/web/20120723052103/http://www.frac.info/frac/index.htm |archive-date=2012-07-23 }}</ref>
-Another method of control is to accelerate the leaf litter decomposition under the trees in citrus groves. Accelerating this decomposition reduces the chance for ascospore inoculation which generally takes place in the middle of March. There are three possible methods to hasten this decomposition. One method is the increase the mircrosprinkler irrigation in the grove to half an hour for at least five days of the week. This form of control should continue for about a month and a half. The second method is to apply urea or ammonium to the leaf litter. The last and final method to accelerate leaf decomposition is to apply lime or calcium carbonate to the litter.  Urea, lime, and calcium carbonate reduce the number of fungal structures and spore production.<ref>{{cite web|url=http://edis.ifas.ufl.edu/cg088|title=PP279/CG088: 2014 Florida Citrus Pest Management Guide: Citrus Black Spot|author1=Megan M. Dewdney |author2=Timothy S. Schubert |author3=Mark R. Estes |author4=Natalia A. Peres |work=ufl.edu|date=2016-05-06}}</ref> Since the fungus requires wet conditions to thrive, air flow in the citrus grove should be maximized to reduce leaf wetness.<ref name="Citrus Black Spot"/>
+Another method of control is to accelerate the [[leaf litter]] decomposition under the trees in citrus groves. Accelerating this decomposition reduces the chance for ascospore inoculation which generally takes place in the middle of March. There are three possible methods to hasten this decomposition. One method is to increase the microsprinkler irrigation in the grove to half an hour for at least five days of the week. This form of control should continue for about a month and a half. The second method is to apply urea or ammonium to the leaf litter. The last and final method to accelerate leaf decomposition is to apply lime or calcium carbonate to the litter.  Urea, lime, and calcium carbonate reduce the number of fungal structures and spore production.<ref>{{cite web|url=http://edis.ifas.ufl.edu/cg088|title=PP279/CG088: 2014 Florida Citrus Pest Management Guide: Citrus Black Spot|author1=Megan M. Dewdney |author2=Timothy S. Schubert |author3=Mark R. Estes |author4=Natalia A. Peres |work=ufl.edu|date=2016-05-06}}</ref> Since the fungus requires wet conditions to thrive, air flow in the citrus grove should be maximized to reduce leaf wetness.<ref name="Citrus Black Spot"/>
-Along with these methods it is also important to get rid of debris such as fallen fruit or twigs in a manner that reduces the chances of infecting other plants. Citrus Black Spot can colonize and reproduce on dead twigs. To dispose of citrus debris it should either be heated to a minimum of 180℉ for two hours, incinerated, buried in a landfill, or fed to livestock. Plant trash should be moved with caution if at all to avoid spreading the infectious ascospores.  Any trees that are infected with citrus black spot should be removed from the grove and disposed of. These trees must be removed because those that are declining and stressed will often have off season bloom. If there is more than one age of fruit present on the tree, it is possible for the asexual spores on the fruit to be transferred to new fruit, intensifying the disease. This off season blooming is often more problematic with Valencia oranges when old and new crops overlap.
+Along with these methods it is also important to get rid of debris such as fallen fruit or twigs in a manner that reduces the chances of infecting other plants. Citrus Black Spot can colonize and reproduce on dead twigs. To dispose of citrus debris it should either be heated to a minimum of 180&nbsp;°F for two hours, incinerated, buried in a landfill, or fed to livestock. Plant trash should be moved with caution if at all to avoid spreading the infectious ascospores.  Any trees that are infected with citrus black spot should be removed from the grove and disposed of. These trees must be removed because those that are declining and stressed will often have off season bloom. If there is more than one age of fruit present on the tree, it is possible for the asexual spores on the older fruits to be transferred to young fruits, thereby intensifying the disease. This off season blooming is often more problematic with Valencia oranges when old and new crops overlap; therefore fruits should be harvested before blooming commences.{{cn|date=November 2022}}
 ==Importance==
-Citrus Black Spot has a large economic impact on many countries because the black blemishes make it undesirable for human consumption and therefore the infected fruit cannot be sold. This type of economic impact is felt most in Australia and South Africa where the disease has been present for a number of years.<ref>[http://www.plantwise.org/?dsid=26154&loadmodule=plantwisedatasheet&page=4270&site=234]{{Dead link|date=July 2019 |bot=InternetArchiveBot |fix-attempted=yes }}</ref> In Australia, South Africa, and China citrus is of particular importance due to the large role it plays in international trade. A few black spots on as little as one piece of fruit can cause the entire shipment to be rejected. When this happens the shipment usually has to be repackaged and resold to a less sensitive market which leads to large financial losses.<ref name=dissertation/> Along with making fruit unsuitable for sale Citrus Black Spot also causes early fruit drop and reduces crop yield.<ref name=aphis /> The reduction in fruit value due to Citrus Black Spot is estimated at 20-30%.<ref>[http://irrec.ifas.ufl.edu/postharvest/pdfs/past_events/2010_presentations/Feichtenberger-CBS.pdf]</ref>
+Citrus Black Spot has a large economic impact on many countries because the black blemishes make it undesirable for human consumption and therefore the infected fruit cannot be sold. This type of economic impact is felt most in Australia and South Africa where the disease has been present for a number of years.<ref>{{Cite web|url=http://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsID=26154|archive-url=https://archive.today/20130415203246/http://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsID=26154|url-status=dead|archive-date=2013-04-15|title=Guignardia citricarpa {{!}} Datasheet {{!}} Plantwise|date=2013-04-15|website=archive.vn|access-date=2020-04-04}}</ref> In Australia, South Africa, and China citrus is of particular importance due to the large role it plays in international trade. A few black spots on as little as one piece of fruit can cause the entire shipment to be rejected. When this happens the shipment usually has to be repackaged and resold to a less sensitive market which leads to large financial losses.<ref name=dissertation/> Along with making fruit unsuitable for sale Citrus Black Spot also causes early fruit drop and reduces crop yield.<ref name=aphis /> The reduction in fruit value due to Citrus Black Spot is estimated at 20-30%.<ref>{{cite web|url=http://irrec.ifas.ufl.edu/postharvest/pdfs/past_events/2010_presentations/Feichtenberger-CBS.pdf|format=PDF|title=Citrus black spot|quotation=Reduction fruit value due to CBS: 20 – 30%|website=Irrec.ifas.ufl.edu|access-date=6 March 2022}}</ref>
-At the end of 2013, the [[European Commission]] announced a ban on most imports of citrus fruit from South Africa because of concerns about the possible transmission of Citrus Black Spot to the EU. This ban was justified by a study by the [[European Food Safety Authority]] (EFSA) on the risk of transmission. However, a specially convened panel of eminent scientists from Brazil, Argentina, the USA, Uruguay, Australia and South Africa concluded that there is no risk of transmission through fruit to European climates. It argued that Citrus Black Spot has never spread to new areas with fruit as the cause and citrus fruit has never been shown to be the cause of the spread of the disease. The panel pointed out that it is known to occur only in summer rainfall citrus production areas and that the only way it has been spread to new areas has been through infected propagation material moved to areas where the climate is suitable for its establishment.<ref>{{cite web|last=Agritrade|title=Debate on Citrus Black Spot continues|url=http://agritrade.cta.int/Agriculture/Commodities/Horticulture/Debate-on-Citrus-Black-Spot-continues|publisher=CTA|accessdate=27 February 2014}}</ref>
+At the end of 2013, the [[European Commission]] announced a ban on most imports of citrus fruit from South Africa because of concerns about the possible transmission of Citrus Black Spot to the EU. This ban was justified by a study by the [[European Food Safety Authority]] (EFSA) on the risk of transmission. However, a specially convened panel of eminent scientists from Brazil, Argentina, the USA, Uruguay, Australia and South Africa concluded that there is no risk of transmission through fruit to European climates. It argued that Citrus Black Spot has never spread to new areas with fruit as the cause and citrus fruit has never been shown to be the cause of the spread of the disease. The panel pointed out that it is known to occur only in summer rainfall citrus production areas and that the only way it has been spread to new areas has been through infected propagation material moved to areas where the climate is suitable for its establishment.<ref>{{cite web|last=Agritrade|title=Debate on Citrus Black Spot continues|url=http://agritrade.cta.int/Agriculture/Commodities/Horticulture/Debate-on-Citrus-Black-Spot-continues|publisher=CTA|access-date=27 February 2014|archive-url=https://web.archive.org/web/20141002211526/http://agritrade.cta.int/Agriculture/Commodities/Horticulture/Debate-on-Citrus-Black-Spot-continues|archive-date=2 October 2014|url-status=dead}}</ref>
 ==See also==
-*[[List of citrus diseases]]
+* [[List of citrus diseases]]
 ==References==
-{{Reflist|30em}}
+{{Reflist}}
 {{citrus}}
 {{Taxonbar|from=Q5615694}}