B.berengeriana f.sp. pyricola is an ascomycete causing leaf spots, warty growths on stems, and “ring rot” of pear [Pyrus] and apple [Malus] fruits in eastern Asia. Morphologically, it is very similar to the “whit...
B.berengeriana f.sp. pyricola is an ascomycete causing leaf spots, warty growths on stems, and “ring rot” of pear [Pyrus] and apple [Malus] fruits in eastern Asia. Morphologically, it is very similar to the “white rot” pathogen of pome fruit, Botryosphaeria dothidea, and the species B.berengeriana itself has been synonymized with that more widespread species, but the production of some different symptoms by the Asian fungus warns of a physiological difference that is not understood or defined and that could still constitute a threat in pome fruit-growing areas where white rot already occurs. No assay, other than by the inoculation of trees, exists to distinguish the fungus easily and quickly from closely-related Botryosphaeria pathogens that might also be carried in fruit or in fruit tree propagating material.
A datasheet on B. berengeriana f.sp. pyricola published by EPPO/CABI (1997b) highlights the doubts about the separate identity of this fungus. An explanation of the taxonomic situation is provided here, but the datasheets on Botryosphaeria ribis and Botryosphaeria dothidea effectively provide a full account of the white-rot disease of pome fruits.
In Japan, the pathogen has been known as Physalospora pyricola since it was described in 1933, although the name Guignardia pyricola (used in the EU Plant Health Directive) was proposed by Yamamoto (1961). However, Guignardia species, have ascospores with a mucus cap and anamorphs of the Phyllosticta type, whereas Botryosphaeria species have larger ascospores without caps and anamorphs in Fusicoccum (Denman et al., 2000). Koganezawa and Sakuma (1980; 1984) compared P. pyricola with another fungus causing fruit rot in Japan, which they called Botryosphaeria berengeriana, and concluded that the two fungi were identical morphologically. The anamorph of B. berengeriana is a Fusicoccum (Sutton, 1980). Recently, B. berengeriana has been considered synonymous with B. dothidea, a fungus that is widespread as a pathogen of many plants in warm temperate regions (von Arx and Müller, 1954; Slippers et al., 2004). However, the Japanese authors regarded it as a synonym of B. ribis, which they and some others consider to be distinct from B. dothidea and which is also widespread in temperate regions. Other authors consider B. dothidea and B. ribis to be synonymous (Brown and Britton, 1986). The disease of pome fruits caused by B. dothidea is called “white rot” (Jones and Aldwinckle, 1990).
As the Japanese isolates of B. berengeriana, previously known as P. pyricola, cause some symptoms (“wart bark”) distinctly different from the cankers due to typical B. berengeriana, Koganezawa and Sakuma (1984) proposed the name B. berengeriana f.sp. pyricola for the fungus causing apple wart bark and B. berengeriana f. sp. persicae for a similar fungus causing blister canker of peaches. These names have not been used outside Japan. Elsewhere in Asia, the agent of apple ring rot has been called B. dothidea (Kim and Kim, 1989), B. berengeriana (Lee and Yang, 1984), or still P. pyricola (Zhang and Huang, 1990). A fungus on apples in Brazil has also been recorded as B. berengeriana (Melzer and Berton, 1986), but the name is probably being used in this case as a simple synonym of B. dothidea. Jones and Aldwinckle (1990) regards B. berengeriana f.sp. pyricola as a synonym of B. dothidea. Furthermore, it is not usual to designate forma specialis to a fungus that attacks species in more than one host genus, and such a name has no status under the rules of nomenclature (Farr et al., 2009).
Slippers et al. (2004) were unable to find morphological differences between the type specimens of B. berengeriana and B. dothidea, but did observe differences between B. dothidea and B. ribis. Comparison of the sequences of the ITS, 5.8S, beta-tubulin and EF1-alpha regions of nuclear DNA supported the latter distinction, but no isolates of B. berengeriana were included in the molecular analysis. On the basis of morphology, then, B. berengeriana was placed in synonymy with B. dothidea. Grouping of fruit tree isolates of Botryosphaeria in Japan by symptoms caused, conidium size, and ITS sequences placed both Physalospora piricola and B. berengeriana f.sp. pyricola together with white-rot-causing B. dothidea isolates from the USA (Ogata et al., 2000). Isolates from fruit trees in Japan were included in the further study of ITS sequences and RFLP patterns by Slippers et al. (2007), which found them to group with isolates of either B. dothidea or the anamorph of Botryosphaeria parva, Neofusicoccum parvum. Thus, while the pathogen population on fruit trees in Japan continues to be complex (Ogata et al., 2000), the identity of the wart bark-causing fungus and the white rot-causing B. dothidea appears confirmed.
Macrophoma kawatsukai and Macrosporium pyrorum have also been listed as anamorphs of B. berengeriana in East Asia (Tai, 1979; Kobayashi, 2007).
According to Koganezawa and Sakuma (1984), the morphology of the fungus is identical to that of Botryosphaeria dothidea. The sizes of the ascoma, asci and ascospores are variable. Asci are 80-130 x 14-23 µm, and ascospores are 19-26 µm long. The conidia, of the Fusicoccum anamorph, are 23-29 x 6-8 µm. In China, conidia of 10 isolates measured 20.0-31.5 x 4.5-7.0 µm (Lee and Yang, 1984).
In the dark, colonies of all isolates on PDA (potato dextrose agar) were initially white, turning grey and then black. In diffuse light (Koganezawa and Sakuma, 1984), isolates of f.sp. pyricola remained grey, whereas isolates of B. dothidea from various hosts (including Malus and Pyrus) were reported to turn yellowish-brown.
Punithalingam and Holliday (1973) have described the morphology of Botryosphaeria ribis, and Jones and Aldwinckle (1990) used the figure from that description in his description of B.dothidea. The anamorph of B. dothidea (Fusicoccum aesculi) is also described by Sutton (1980).
Slippers et al. (2004) were unable to find morphological differences between the type specimens of B. berengeriana and B. dothidea; tables presenting their observations on these species and on B. ribis and Botryosphaeriaparva are included in their report.
Strictly speaking, B. berengeriana f.sp. pyricola has only been recorded in Japan, except that the name has also been used in recent publications from China. Apple ring rot (under various names for the pathogen) has been recorded from several East Asian countries (China, Japan, Korea, and Taiwan) (CABI/EPPO, 1998). The white rot pathogen Botryosphaeriadothidea, on the other hand, occurs very widely (Sutton, 1990). In the absence of a universally agreed-upon taxonomy, geographical distribution cannot be reported meaningfully. The name B. berengeriana has also been used for an apple pathogen in Brazil (Melzer and Berton, 1986), but presumably this refers to B. dothidea, given that cankers, rather than warts, are the symptom on stems (see Valdebenito-Sanhueza et al., 2005).
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
No regional plant protection organization has considered B. berengeriana f.sp. pyricola to be a quarantine pest, but it is listed in the regulations of the European Union, and also those of the USA (EPPO/CABI, 1997b). Although mainly occurring on Pyrus pyrifolia in Japan, the fungus has been recorded damaging Pyrus communis (Kobayashi, 2007). In other countries, apple [Malus spp.] is the crop of primary concern (Lee and Yang, 1984; Zhao et al., 1998). In Japan, B. berengeriana f.sp. pyricola has been thought to be more important than Botryosphaeria dothidea and to cause different symptoms. So, in principle, apple- and pear-growing countries around the world are at risk. However, different names for the pathogens are used in different countries, and it is not clear whether all the published information refers to the same fungus, or whether B. berengeriana f.sp. pyricola can really be distinguished from B. dothidea, or how feasible it might be to take regulatory measures against a physiologically specialized form alone. In addition, it may be noted that the Japanese fungus, like B. dothidea in south-eastern USA (Brown and Britton, 1986), is favoured by rather warmer and more humid conditions than those that prevail in most apple- and pear-growing areas (EPPO/CABI, 1997b). Thus, the phytosanitary risks from this fungus are very debatable.
The main host is Japanese pear (Pyrus pyrifolia), but European pear (Pyrus communis) and apple [Malus spp.] are also attacked. Other hosts mentioned by Kato (1973) are Chaenomeles japonica and Malus micromalus. Ogata et al. (2000) identified a group of similar pathogenic isolates that included B. berengeriana f. sp. pyricola; hosts for these Japanese isolates included grapevine [Vitis vinifera] and peach [Prunus] as well as apple and pear.
On Japanese pears [Pyrus pyrifolia] (Kato, 1973) and apples [Malus] in China (Lee and Yang, 1984), the fungus forms wart-like protuberances (wart bark) on the surface of trunks and branches, rather than typical Botryosphaeria cankers. These are subsequently surrounded by dark-brown spots. Infected twigs eventually wither and die back. Large contoured dark-brown spots are formed on the leaves and the fruits. The warts on trunks and branches damage the tree, reducing its growth and productivity. The leaf spots are of minor importance and do not affect yield.
Fruit spots are circular, slightly sunken, and may be surrounded by a red halo; alternating light- and dark-brown rings develop as the lesions enlarge (Jones and Aldwinckle, 1990). The fruit spots develop further after harvest (Al-Haq et al., 2002; 2003), and thus cause a loss of fruit quality.
B. berengeriana f.sp. pyricola infects the branches, shoots, leaves and fruits of its hosts. Stroma containing conidiomata form on diseased branches and shoots after these have withered, during the period from April to September, but mainly in August and September (Dong and Zhou, 1985; Koga and Ohkubo, 1994). Sporulation is most abundant on two- to three-year-old infected shoots and less on older wood. The conidia are rain-dispersed, usually up to about 10 m, but exceptionally up to 20 m by strong wind-driven rain. Most germinate within the first 24 h, and infection is favoured by warm humid conditions (optimum temperature 28°C). Infection of young fruits requires 5 h of surface wetness, whereas a longer period is needed on older fruits (Koga and Ohkubo, 1994).
Under experimental conditions, artificial wounding is needed for infection of branches, although shoot tips and young leaves can be infected in the absence of wounds. 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 and Abiko, 1971; Dong and Zhou, 1985). Thereafter, wounds, such as the punctures made by Grapholita molesta, the oriental fruit moth, are needed for infection of fruits (EPPO/CABI, 1997a).
The incubation period for infection of shoots is 90-120 days, so that shoots infected during April-August show symptoms in September-November, and will provide inoculum in the following year. Leaves are infected from July to 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 using a quadratic regression equation (Kato, 1973).
Ascomata are found on withered branches, but ascospores are not reported to play a significant role in disease spread.
This description of the biology of B. berengeriana f.sp. pyricola is taken from the Asian literature. However, it is very broadly similar to that of Botryosphaeria dothidea, for example in the south-eastern USA (McGlohon, 1982; Brown and Britton, 1986; Jones and Aldwinckle, 1990), or in Korea (Kim and Kim, 1989).
As Physalospora pyricola, the fungus was listed as one of the economically important pests of apples [Malus] and pears [Pyrus] in Japan (Anon., 1984), being responsible for branch dieback (of the “mal secco” type) and fruit rot. According to Koganezawa and Sakuma (1984), it became even more important, causing apple fruit rot in the 1980s, after Bordeaux mixture [copper sulphate and lime] was less frequently used in orchards and the practice of bagging fruits had declined. (In Japan, high quality pome fruits are often individually bagged on the tree to protect them from all kinds of damage). Presumably, the fungus was previously controlled well with copper fungicides.
Losses of up to 50% in susceptible cultivars of apples were reported in China (Kexiang et al., 2002).
Botryosphaeria dothidea, in the wide sense, also causes a branch canker of pome fruit trees, and white rot of fruits. It is not regarded as very important over most of its range, but has been more severe in the south-eastern USA, where losses could be as high as 100% (Brown and Britton, 1986; Sutton, 1990).
Sassa et al. (1998) identified antifungal compounds produced by a fungus identified as B. berengeriana. The macrophorins E, F and G inhibited growth of both the producing species and Gibberella fujikuroi, a pathogen of rice.
No DNA sequence linked to a published report has been deposited in GenBank for B. berengeriana f.sp. pyricola (NCBI, 2009). Sequences for strains identified as causing the wart symptom by Ogata et al. (2000) are deposited as Botryosphaeria dothidea.Slippers et al. (2007) report a protocol for distinguishing among Botryosphaeria species from fruit trees using a RFLP map based on results with two restriction enzymes. Vilas-Boas et al. (2007) found that 200 bp sequences from the beginning of ITS 1 or the end of ITS 2 were the minimum necessary to distinguish among 11 of 13 species of Botryosphaeria.
The symptoms caused on pear [Pyrus] and apple [Malus] twigs and stems include warts and dieback. The fungus may or may not fruit in lesions, producing straight hyaline aseptate fusiform conidia in locules contained in a dark stroma (Sutton, 1980).
If they are distinct species, B. berengeriana, Botryosphaeria dothidea and Botryosphaeria ribis are very similar in morphology and can be difficult to distinguish. Slippers et al. (2004) were unable to find morphological differences between the type specimens of B. berengeriana and B. dothidea, but did report morphological differences in B. ribis. As a physiologically specialized variant, B. berengeriana f.sp. pyricola 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, produced conidia within a certain size range, and could be distinguished by the sequence of the ITS rDNA region. The group included isolates identified as Physalospora piricola, B. berengeriana f.sp. pyricola, or B. dothidea. Other isolates had smaller or larger conidia and different ITS sequences.
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Unless a specific test is found for the Japanese or Asian isolates of the pathogen, particular exclusion of the specialized form of the fungus will not be feasible when materials not exhibiting the “wart bark” symptom are involved. Nevertheless, even though Botryosphaeria dothidea may be present already as a pathogen of fruit trees in a particular region, exclusion of foreign strains, which may differ in host range, aggressiveness or resistance to pesticides, should still be enforced.
Cultural Control and Sanitary Measures
In general, measures to reduce the conidial inoculum are recommended. Branches showing symptoms of infection should be pruned. The warts on shoots can be shaved away. Affected fruits should be removed and destroyed.
Al-Haq et al. (2002) found that EO (electrolyzed oxidizing) water reduced, but did not, eliminate post-harvest rot in pears [Pyrus]. Hot water treatment, on the other hand, consisting of immersion of fruit for 3 minutes at 54°C, did reduce disease incidence by 85% in experimental trials in Japan (Al-Haq et al., 2003). It was noted that this is unlikely to be effective against deeper wounds, especially those that become inoculated during harvest.
As the frequent application of fungicides has resulted in the development of resistance in the pathogen, Kexiang et al. (2002) investigated the use of Trichoderma species for the control of ring rot of apple. Treatment with suspensions of conidia of Trichoderma harzianum T88 or Trichoderma atroviride T95 reduced both the incidence and severity of the disease, as well as reducing the survival of the fungus, in detached branch sections. Disease on stems and fruit of orchard trees was reduced to a level similar to that obtained with regular applications of Bordeaux mixture [copper sulphate and lime] and carbendazim. Other efforts at biological control in China have involved application of the bacterium, Bacillus subtilis (Zhao et al., 1998) and an antibiotic (Zhu et al., 2004).
Copper fungicides have proved effective in Japan, and the reduction in their use has led to a resurgence of apple fruit rot. Benomyl, captan, polyoxin and 8-hydroxyquinoline are other fungicides that have been shown to be effective in Japan (Kishi and Abiko, 1971; Kato, 1973). Both the copper-containing Bordeaux mixture and the organic carbendazim are used in China (Kexiang et al., 2002). Organic fungicides are recommended against B. dothidea in the USA (McGlohon, 1982) and Korea (Kim and Kim, 1989). Sato et al. (1987) have recently investigated eradicant fungicides for trunk lesions.
An assay is needed to distinguish the physiologically different fungus easily and quickly from closely related Botryosphaeria pathogens that might also be carried in fruit or in fruit tree propagating material. This assay will likely also elucidate the nature of the difference in the Asian pathogen, as well as allowing for a clear determination of its geographic distribution.
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Zhao BG, Kong J, Wang WX, Shen XC, 1998. Suppression of apple ring rot pathogen (Physalospora piricola) by Bacillus subtilis and its effect in field control. In: Acta Phytopathologica Sinica, 27 (3) 213-214.