Preferred name: Botryosphaeria kuwatsukai
Authority: (Hara) G.Y. Sun & E. Tanaka
Taxonomic position: Fungi: Ascomycota: Pezizomycotina: Dothideomycetes: Botryosphaeriales: Botryosphaeriaceae
Other scientific names: Botryosphaeria berengeriana f. sp. pyricola (Nose) Koganezawa & Sakuma, Guignardia pyricola (Nose) Yamamoto, Macrophoma kuwatsukai Hara, Macrophoma pyrorum Cooke, Physalospora pyricola Nose
Common names in English: blister canker of pome fruits, physalospora canker of pome fruits, ring rot of apple, wart bark of apple
view more common names online...
Notes on taxonomy and nomenclature EU Categorization: A1 Quarantine pest (Annex II A)
view more categorizations online...
EPPO Code: PHYOPI

The main host is Japanese pears (Pyrus pyrifolia), but European pears (P. communis) and apples (Malus spp.) are also be affected (Xu et al., 2015). Other hosts are Chaenomeles japonica and Malus micromalus which were mentioned by Kato (1973) and Cydonia oblonga (CABI, 2023), but no additional references were found to confirm susceptibility of these plants to the pathogen, so there is still uncertainty about these hosts (Jayasiri et al., 2015; EFSA, 2017).

Host list: Chaenomeles japonica, Cydonia oblonga, Malus domestica, Malus x micromalus, Pyrus communis, Pyrus pyrifolia var. culta

B. kuwatsukai has been recorded only from Eastern Asia and has not apparently widely spread from there. The name B. berengeriana has also been used for an apple pathogen in Brazil, but presumably refers to B. dothidea.

Asia: China (Anhui, Fujian, Guangxi, Hebei, Henan, Hubei, Jiangsu, Jiangxi, Jilin, Liaoning, Shaanxi, Shandong, Shanxi, Sichuan, Zhejiang), Japan (Honshu, Shikoku), Korea Dem. People's Republic, Korea, Republic, Taiwan

B. kuwatsukai infects branches, shoots, leaves and fruits of its hosts. The fungus causes large cankers and bark blisters on pear (Pyrus communis), whereas on apple shoots, it induces large wart-like bark swellings (Xu et al., 2015). The disease is characterized by black pycnidial stromata that differentiate beneath the surface of killed bark and break through at maturity (Sinclair & Lyon, 2005). Stromata vary in shape, pycnidia form on diseased branches and shoots after these have withered, during the period from April to September, but mainly in August and September (Ogata et al., 2000; EPPO, 2023). Sporulation is most abundant on infected shoots which are 2–3 years old and less on older wood (Sinclair & Lyon, 2005). Under wet weather conditions when infected bark is moist, one-celled, colourless conidia 17–25 x 5–7 µm, somewhat narrowed at each end, extrude in a white mass from the pore at the top of each pycnidium (Sinclair & Lyon, 2005). The conidia are rain-dispersed, usually up to about 10 m, but exceptionally up to 20 m by strong wind-driven rain (Sinclair & Lyon, 2005). They mostly germinate within 24 h, and the peak of conidia release occurs after 4 h of moisture retention and maintains a high level for 12 h (Shutong et al., 2012). The infection is favoured by warm humid conditions (optimum temperature 28°C) and infection of young fruits requires 5 h of surface wetness, while older fruits need longer (Shutong et al., 2012).

The pycnidial stromata develop throughout the year as temperature permits, usually beginning within days to weeks after diseased tissues die and stromata development depends upon sufficient moisture in the killed tissues (Sinclair & Lyon, 2005).

Under experimental conditions, artificial wounding is needed for branches to be infected, although shoot tips and young leaves can be infected without wounding. Natural infection of shoots probably occurs through the shoot tip. Similarly, young fruits can be infected early in the season (up to mid-July) through stomata or lenticels (Kishi & Abiko, 1971). Thereafter, wounds are needed for infection of fruits (e.g. punctures of Grapholita molesta; EPPO/CABI, 1996).

The incubation period for infection of shoots is 90–120 days, so that shoots infected during April–August show symptoms in September–November and provide inoculum in the following year. Leaves are infected in July–August, with an incubation period of about 30 days. The occurrence of the disease on fruits can be predicted from the number of rainy days in May by a quadratic regression equation (Kato, 1973).

Mature pseudothecia of the sexual stage may develop in the same stromata that previously produced conidia or in new stromata, usually on tissue which has been dead for several months to a year or more (Sinclair & Lyon, 2005). When pseudothecia are developed, ascospores are dispersed by air and water during much of the growing season and, like conidia, are most abundant during late spring to early summer, but ascospores are not reported to play a significant role in disease spread (Sinclair & Lyon, 2005).

Morphologically, however, it is hard to discriminate B. kuwatsukai from B. dothidea as they produce similar conidia and affected the same hosts inducing similar symptoms (Xu et al., 2015).

B. kuwatsukai can exist as endophyte in healthy plant tissues for extended period of time (Slippers et al., 2017).

This description of the biology of B. kuwatsukai is taken mostly from the old Japanese literature; it is, however, very broadly similar to that of B. dothidea, for example in South-Eastern USA (McGlohon, 1982; Koganezawa & Sakuma, 1984; Brown & Britton, 1986; Jones & Aldwinkle, 1990).

Symptoms

Symptoms caused by B. kuwatsukai may vary in size and extent on apple and pear trees (Sinclair & Lyon, 2005, Dong et al., 2021). The disease characterized by ring rot on fruit and restricted warts on branches is known as ring rot because of the alternating light and dark concentric rings in the fruit rot lesions (Dong et al., 2021). On Japanese pears and apple (Malus spp.), the fungus forms wart-like protuberances (wart bark) on the surface of trunks and branches, rather than typical Botryosphaeria cankers (Jones, 2014). The warts on trunks and branches damage the tree, reducing its growth and productivity. Lesions on branches, twigs and trunk vary from tiny and superficial spots on bark to sunken cankers delimited by vigorous callus ridges or spreading lesions without marginal callus (Sinclair & Lyon, 2005; Jones, 2014, Dong et al., 2021). Usually, infected twigs die, but trunks and branches may have no symptoms or contain the pathogen within discrete cankers (Sinclair & Lyon, 2005; Jones, 2014). The leaf spots are of minor importance and do not affect yield. The fruit spots progress after harvest, alternating light and dark brown rings develops in the decayed tissue, and thus cause a loss of fruit quality (Koganezawa & Sakuma, 1980, 1984).

To distinguish B. kuwatsukai and B. dothidea, pathogenicity tests could be used showing that on pear stems B. kuwatsukai caused large-scale cankers along with blisters whereas B. dothidea was non-pathogenic (Xu et al., 2015). There are two distinct symptoms on apple (Malus domestica) that can be also used to distinguish B. kuwatsukai and B. dothidea. The first one is causing ring rot on fruit and restricted wart-like prominences or canker-like protrusions the year after infection, while the other causes expanding cankers on branches (Dong et al., 2021).

Morphology

According to Xu et al. (2015), most of morphological features of the fungus are identical to those of B. dothidea. Xu et al. (2015) also provide the following description of the cultural and morphological characteristics of B. kuwatsukai: colonies on potato dextrose agar (PDA) media attaining 52 mm diameter after 4 days at 25°C in the dark, initially white with moderately dense, appressed mycelial mat and aerial mycelium without columns, gradually becoming grey to dark grey (Jayasiri et al., 2015). The reverse side of the colonies at first is white, but after 2–3 days it becomes dark green to olive-green from the centre. This colouration gradually spreads to the edge and becomes darker from the centre until the entire underside of the colony is black (Jayasiri et al., 2015). Conidiomata in culture are superficial, dark brown to black, globose, mostly solitary and covered by mycelium (Jayasiri et al., 2015). Conidiogenous cells holoblastic, hyaline, sub-cylindrical, 7–18 × 2–4 μm, conidia produced in culture similar to those formed in nature, narrowly fusiform, or irregularly fusiform, base subtruncate to bluntly rounded, smooth with granular contents, widest in the middle to upper third, (18.5–)20…24.5(–26) × 5…7(–8) μm (mean ± SD = 22.3 ± 2.1 × 6.2 ± 0.9 μm, n = 60, L/W ratio = 3.6), forming 1–3 septa before germination (Jayasiri et al., 2015). The pycnidial stromata in nature vary in size, they are 1–4 mm in the longest dimension and contain one to several pycnidial cavities 150–250 µm in diameter with colourless contents that appear white when sliced (Sinclair & Lyon, 2005). Microconidiomata globose, dark brown to black. Microconidiophores hyaline, cylindrical to sub-cylindrical, 3–10 × 1–2 μm, microconidia unicellular, hyaline, allantoid to rod-shaped, 3–8 × 1–2 μm. Sexual state not observed in culture (Jayasiri et al., 2015).

Detection and inspection methods

B. kuwatsukai, which has for many years been confused with B. dothidea, can be identified based on multiple methods. Biological characteristics including the aerial mycelia growth, mycelial growth rate and pathogenicity also supported the segregation of these two species. Morphologically, however, it is difficult to discriminate B. kuwatsukai from B. dothidea as they produce similar conidia. As a physiologically specialized taxon, B. kuwatsukai has only been distinguished by the different symptoms, warts rather than cankers, that it causes on twigs and stems of apple (Malus spp.). Examining a number of Botryosphaeria isolates from fruit trees in Japan, Ogata et al. (2000) found a group that caused the wart symptom on twigs, size of the conidia within a certain size range, and could be distinguished by the nucleotide sequences of rDNA ITS 1, ITS 2 and 5.8S rDNA. Molecular data are available in GenBank for the epitype of B. kuwatsukai, HMAS 245112 (PG 2) and GenBank contains sequences of different region: ITS: KJ433388 (ITS1/ITS4); EF1-α: KJ433410 (EF446f/EF1035r); HSP: KJ433456 (HspF3/HspR); HIS: KJ433432 (HisF3/HisR) (Jayasiri et al., 2015).

Imported host plants for planting and dormant plants of apple (Malus spp.) and pear (Pyrus spp.) trees from the countries where the disease occurs should not have any symptoms of cankers and bark blisters or wart-like bark swellings cankers on apple and Japanese pear during inspection.

Any material with canker lesions should be carefully inspected. Particular attention should be paid to the fruit (apples and pears) because they can have black conidiomata scattered on the lesions (Jayasiri et al., 2015). Infection occurs on young fruit, and would be detectable on harvested fruit, rather than only appearing later in storage (post-harvest rot). Accordingly, infected fruit are relatively unlikely to be traded. However, it is possible that pathogen can survive in symptomless branches and trunks which may contain mycelium or stromata, thus inspection may be ineffective.

The pathogen can spread by both natural and human-assisted means. Under natural conditions, B. kuwatsukai is locally dispersed by rain over relatively short distances. Nevertheless, uncertainty exists on the distance over which the ascospores of the pathogen could be wind disseminated because of lack of information (EFSA, 2017). The fungus can potentially spread over long distances through the movement of infected (symptomatic and asymptomatic) timber, bark, plants for planting (rootstocks, grafted plants, scions, etc.), and fresh fruit (EFSA, 2017), although it seems improbable that infected fruit could be traded. As mentioned above, B. kuwatsukai can exist as endophyte in healthy plant tissues for extended periods of time, thus it can potentially spread freely with healthy plant material, including fruit (Slippers et al., 2017).

Economic impact

B. kuwatsukai is the pathogen responsible for apple ring rot and pear canker and it can cause rot on fruit, especially during storage, and extensive cankers and/or warts on branches and trunks, resulting in serious economic losses to fruit farmers in China, Japan, and Koreas on apple and Japanese and European pears (Ogata et al., 2000; Jayasiri et al., 2015; Zhao et al., 2015, Dong et al., 2021). According to Koganezawa & Sakuma (1984), it has become more common, causing apple fruit rot in the 1980s, when Bordeaux mixture began to be used less frequently in orchards and the practice of bagging fruits declined (in Japan, high quality pome fruits are often individually bagged on the tree to protect them from all kinds of damage). A survey in 2008 in the seven main apple production provinces in China has showed that the average incidence of apple ring rot was 77.6% (Dong et al., 2021).

Control

Copper fungicides have proved effective in Japan, and the reduction in their use has led to a resurgence of apple fruit rot (Kexiang et al., 2002; Bhusal et al., 2016). Organic arsenic emulsion was previously recommended in Japan for treatment of the warts on the shoots, though it is doubtful whether such products would now be authorized for this use (Liu et al., 2011).

Biological control of this pest has also been tested. Laboratory and field trials were carried out in Hebei province (China) to evaluate the potential of Trichoderma harzianum and T. atroviride (Ascomycota: Hypocreaceae) to control B. kuwatsukai. In the laboratory, both Trichoderma species inhibited the B. kuwatsukai, apparently by direct antagonism with minor inhibition by antibiosis. In the field, where apple trees were severely affected by the disease, the application of spore suspensions of both fungi gave satisfactory results and the efficacy was similar to that of routine chemical control (Kexiang et al., 2002).

In general, it is recommended to take the following agricultural practices and sanitary and chemical measures to reduce the inoculum source: pruning of symptomatic and dead plant parts and shaving of warts on shoots; sprays with copper-based fungicides; sanitation measures to reduce inoculum sources in the orchards (Cho et al., 1986; Kim & Kim, 1989; EFSA, 2017).

Phytosanitary risk

B. kuwatsukai has never been reported in the EPPO region. In Japan, China, and Koreas the fungus is reported to be important. Though mainly occurring on Japanese pears, the fungus has been recorded in Japan damaging European pears and apples. The risk of entry (for the EU) was assessed by EFSA as the pest could potentially enter, establish and spread in the EU. It is not clear, however, whether the fungus can be distinguished from B. dothidea during inspection, and how feasible it is to take measures if the pest identification is difficult (EFSA, 2017).

Phytosanitary measures were suggested to prevent the entry of the pathogen into the EPPO region (e.g. sourcing host plants for planting and fruit should originate from pest-free areas or pest-free places of production). In the case of B. kuwatsukai, inspections at the place of origin and the entry point might be not fully effective to prevent the entry of the pathogen because of it is difficult to ensure that imported plants for planting of Malus and Pyrus from countries where the pathogen is known are free from a latent infection As a general approach, it has also been recommended that when importing plants for planting (except seeds) from the countries where B. kuwatsukai occurs, precautions should have been taken to avoid any infestations while the plants or fruits are transported through possibly infested areas (Kim & Kim, 1989; EFSA, 2017).

Bhusal N, Kwon JH, Han SG & Yoon TM (2016) Applications of organic fungicides reduce photosynthesis and fruit quality of apple trees. Horticultural Science and Technology 34(5), 708-718. https://doi.org/10.12972/kjhst.20160074

Brown EA & Britton KO (1986) Botryosphaeria diseases of apple and peach in the southeastern United States. Plant Disease 70, 484–484.

Cho WD, Kim CH & Kim SC (1986) Pathogen specialization, epidemiology and varietal resistance in white rot of apple. Korean Journal of Plant Protection 25, 63–70.

Dong GZ & Zhou JM (1985) [Observations on the infection period of ring rot on both branches and trunks of apple tree and on the period of conidial dispersal]. Shanxi Fruit Trees 19, 37–39.

Dong XL, Cheng ZZ, Leng WF, Li BH, Xu XM, Lian S & Wang CX (2021) Progression of symptoms caused by Botryosphaeria dothidea on apple branches. Phytopathology 111(9), 1551-1559. https://doi.org/10.1094/PHYTO-12-20-0551-R

EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, ... & Rossi V (2017) Pest categorisation of Botryosphaeria kuwatsukai. EFSA Journal 15(11), e05035. https://doi.org/10.2903/j.efsa.2017.5035

Farr DF, Bills GF, Chamuris GP & Rossman AY (1989) Fungi on Plants and Plant Products in the United States, pp. 592–593. American Phytopathological Society, St. Paul, Minnesota, USA.

Jayasiri SC, Hyde KD, Ariyawansa HA, Bhat J, Buyck B, Cai L, Dai YC, Abd-Elsalam KA, Ertz D, Hidayat I, Jeewon R, Jones EBG, Bahkali AH, Karunarathna SC, Liu JK, Luangsa-ard JJ, Lumbsch HT, Maharachchikumbura SSN, McKenzie EHC, Moncalvo, JM, Ghobad-Nejhad M, Nilsson H, Pang KA, Pereira OL, Phillips AJL, Raspé O, Rollins AW, Romero AI, Etayo J, Selçuk F, Stephenson SL, Suetrong S, Taylor JE, Tsui CKM, Vizzini A, Abdel-Wahab MA, Wen TC, Boonmee S, Dai DQ, Daranagama DA, Dissanayake AJ, Ekanayaka AH, Fryar SC, Hongsanan S, Jayawardena RS, Li WJ, Perera RH, Phookamsak R, de Silva NI, Thambugala KM, Tian Q, Wijayawardene NN, Zhao RL, Zhao Q, Kang JC & Promputtha I (2015) The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Diversity 74(1), 3–18. https://doi.org/10.1007/s13225-015-0351-8

Jones AL (2014) Compendium of Apple and Pear Diseases (2nd ed.). American Phytopathological Society, St. Paul, Minnesota, USA.

Kato K (1973) Studies on physalospora canker of Japanese pear with special reference to ecology and control. Special Research Bulletin of the Aichi-Ken Agricultural Research Center Nagakute, Aichi, Japan, Series B, pp. 1–70.

Kexiang G, Xiaoguang L, Yonghong L, Tianbo Z & Shuliang W (2002) Potential of Trichoderma harzianum and T. atroviride to control Botryosphaeria berengeriana f. sp. piricola, the cause of apple ring rot. Journal of Phytopathology 150, 271–276. https://doi.org/10.1046/j.1439-0434.2002.00754.x

Kim SB & Kim CS (1989) [Pathogenicity and ecology of apple rot caused by Botryosphaeria dothidea. II. The ecology and control methods of apple rot]. Journal of the Korean Society for Horticultural Science 30, 129–136.

Koganezawa H & Sakuma T (1980) Fungi associated with blister canker and internal bark necrosis of apple trees. Bulletin of the Fruit Tree Research Station Japan, Series C 7, 83–99.

Koganezawa H & Sakuma T (1984) Causal fungi of apple fruit rot. Bulletin of the Fruit Tree Research Station Japan, Series C 11, 49–62.

Lee DH & Yang JS (1984) [Studies on the white rot and blister canker in apple trees caused by Botryosphaeria berengeriana]. Korean Journal of Plant Protection 23, 82–88.

Li WJ, McKenZie EHC, Liu JK, Bhat DJ, Dai DQ, Caporesi E, Tian Q, Maharachcikumbura SSN, Luo ZL, Shang QJ, Zhang JF, Tangthirasunun N, Karunarathna SC, Xu JC & Hyde KD (2020) Taxonomy and phylogeny of hyaline-spored coelomycetes. Fungal Diversity 100, 279–801.

Liu HT, Li CL, Zhang YJ, Li CM, Zhao YB, Chen DM, Zhang XZ & Han ZH (2011) Inheritance and molecular marker of resistance to bot canker in Malus domestica. Agricultural Sciences in China, 10(2), 175-184. https://doi.org/10.1016/S1671-2927(09)60304-7

Melzer RR & Berton O (1986) [Incidence of Botryosphaeria berengeriana on apple in the State of Santa Catarina, Brazil]. Fitopatologia Brasileira 11, 891–898.

Ogata T, Sano T & Harada Y (2000) Botryosphaeria species isolated from apple and several deciduous fruit trees are divided into three groups based on the production of warts on twigs, size of conidia, and nucleotide sequences of nuclear ribosomal DNA ITS regions. Mycoscience 41, 331–337. https://doi.org/10.1007/BF02463946

Sinclair WA & Lyon HH (2005) Diseases of Trees and Shrubs (2nd ed.). Comstock Publishing Associates. 650 pp.

Shutong W, Wang Y, Hu T & Cao K (2012) Crucial weather conditions for conidia release of Botryosphaeria berengeriana De Not. f. sp. piricola on apple stems. Acta Horticulturae 940, 701–706.

Slippers B, Crous PW, Jami F, Groenewald JZ & Wingfield MJ (2017) Diversity in the Botryosphaeriales: Looking back, looking forward. Fungal Biology 121, 307–321. https://doi.org/10.1016/j.funbio.2017.02.002

Wang B, Liang X, Gleason ML, Zhang R & Sun G (2018) Comparative genomics of Botryosphaeria dothidea and B. kuwatsukai, causal agents of apple ring rot, reveals both species expansion of pathogenicity-related genes and variations in virulence gene content during speciation. IMA Fungus 9, 243–257. https://doi.org/10.5598/imafungus.2018.09.02.02

Wang B, Liang X, Hao X, Dang H, Hsiang T, Gleason ML, Zhang R & Sun G (2021) Comparison of mitochondrial genomes provides insights into intron dynamics and evolution in Botryosphaeria dothidea and B. kuwatsukai. Environmental Microbiology 23(9), 5320–5333. https://doi.org/10.1111/1462-2920.15608

Xu C, Wang C, Ju L, Zhang R, Biggs AR, Tanaka E, Li B & Sun G (2015) Multiple locus genealogies and phenotypic characters reappraise the causal agents of apple ring rot in China. Fungal Diversity 71, 215–231.

Yamamoto W (1961) [Species of the genera of Glomerella and Guignardia with special reference to their imperfect stages]. Scientific Reports of the Hyogo University of Agriculture, Agricultural Biology 25, 1–12.

Zhao X, Zhang G, Li B, Xu X, Dong X, Wang C & Li G (2016) Seasonal dynamics of Botryosphaeria infections and symptom development on apple fruits and shoots in China. European Journal of Plant Pathology 146, 507–518. https://doi.org/10.1007/s10658-016-0935-5

EFSA resources used when preparing this datasheet

EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, ... & Rossi V (2017) Pest categorisation of Botryosphaeria kuwatsukai. EFSA Journal, 15(11), e05035. https://doi.org/10.2903/j.efsa.2017.5035

This datasheet was extensively revised in 2023 by Kateryna Davydenko, Ukrainian Research Institute of Forestry and Forest Melioration and Swedish University of Agricultural Science. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Botryosphaeria kuwatsukai. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-26)

This datasheet was first published as Botryosphaeria berengeriana f. sp. piricola in the first edition of 'Quarantine Pests for Europe' in 1992 and revised in the second edition of the book in 1997, as well as in 2023. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).