Preferred name: Elsinoë australis
Authority: Bitancourt & Jenkins
Taxonomic position: Fungi: Ascomycota: Pezizomycotina: Dothideomycetes: Dothideomycetidae: Myriangiales: Elsinoaceae
Other scientific names: Elsinoe australis Bitancourt & Jenkins, Sphaceloma australis Bitancourt & Jenkins, Sphaceloma fawcettii var. viscosa Jenkins
Common names in English: scab of sweet orange
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Notes on taxonomy and nomenclature EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: ELSIAU

E. australis is most important on oranges (C. sinensis) and mandarins (C. reticulata) causing fruit scab but not affecting leaves (Timmer et al., 2000). It also infects fruits of sour oranges (C. aurantium), lemons (C. limon), satsumas (C. unshiu), limes (C. aurantiifolia), grapefruits (C. paradisi), tangor (Citrus x nobilis), satsuma (Citrus unshiu), calamondin (x Citrofortunella microcarpa), natsudaidai (C. natsudaidai), and Fortunella (Fortunella sp., Fortunella margarita). In contrast to E. fawcettii, E. australis is known to occur, in addition to citrus and allies Rutaceae species, on other plant species in different families (e.g. Simmondsiaceae, Salicaceae). In Australia, Ash et al. (2012) reported a new pathotype of E. australis causing a black scab disease of jojoba (Simmondsia chinensis). In south-eastern China, Zhao et al. (2020) reported that E. australis is causing a spot anthracnose on poplar (Populus tomentosa and P. deltoides) leaves. Poplar isolates of E. australis were able to cause scab symptoms on the fruit of one hybrid citrus but not on fruit of orange, lemon, or grapefruit.

Host list: Citrus australasica, Citrus hystrix, Citrus natsudaidai, Citrus reticulata, Citrus trifoliata, Citrus x aurantiifolia, Citrus x aurantium var. deliciosa, Citrus x aurantium var. paradisi, Citrus x aurantium var. sinensis, Citrus x aurantium var. unshiu, Citrus x aurantium, Citrus x limon, Citrus x limonia var. jambhiri, Citrus x nobilis, Fortunella margarita, Populus deltoides, Populus tomentosa, Simmondsia chinensis, x Citrofortunella microcarpa

E. australis has a very restricted distribution compared to E. fawcettii. It originally occurred only in South America (Chung, 2011), but its presence on citrus in southern USA and Asia (Japan and the Republic of Korea) has recently been confirmed. E. australis was first detected in Japan in 2012 as the Natsudaidai pathotype on satsuma mandarin, navel orange and a hybrid of natsudaidai and orange (Hyun et al., 2007). South Korean isolates of E. australis also belong to Natsudaidai pathotype (Hyun et al., 2001). In Australia, E. australis has been reported on jojoba (Simmondsia chinensis) but not on citrus (Miles et al., 2015). In south-eastern China, E. australis has been detected causing a leaf disease on poplar (Zhao et al., 2020) but is not known to occur on citrus. At present (as of September 2020), E. australis is absent from the EPPO region. In the literature, there is an old record from Sicily (Ciccarone, 1957) but the fungus has never been there found again.

Asia: China (Anhui, Jiangsu), Japan (Honshu), Korea, Republic
North America: United States of America (Alabama, Arizona, California, Florida, Louisiana, Mississippi, Texas)
South America: Argentina, Bolivia, Brazil (Goias, Minas Gerais, Rio de Janeiro, Rio Grande do Sul, Sao Paulo), Paraguay, Uruguay
Oceania: Australia (New South Wales, Queensland)

Inoculum for new infections consists mainly of conidia. These are produced in the acervuli on the surface of scab lesions on young fruits and leaves throughout the year. E. australis produces only hyaline, one-celled, elliptical conidia and does not produce spindle-shaped conidia in scab lesions (those are only produced by E. fawcettii). Survival and infectious ability of conidia are reliant on wet conditions, quickly dying if exposed to dry conditions. Conidia are formed abundantly on wet scabs, in a nearly saturated atmosphere at optimum temperature between 20 and 28°C. Dispersal of E. australis is mostly by rain or irrigation water. Insects and, to a certain extent, wind-carried water droplets containing spores may also contribute to the spread (CABI, 2020). Infection severity depends on the available inoculum load and the incidence of wetting periods. Germination of conidia and infection do not require liquid water, both processes being possible with dew, fog or under high moisture conditions. A minimum wetness period of 1-2 h is needed for sporulation while a wet period of 2.5-3.5 h is needed for conidial infection (Timmer, 2000). Scab incidence is usually much higher in low-lying areas with frequent wetting, compared to elevated areas (Chung, 2011). The temperature range required for germination of conidia is 13-32°C, but infection does not take place below 14°C or above 25°C (Whiteside, 1975). The incubation period is of at least 5 days. The optimal temperature for disease development is 20-21°C (Timmer, 2000). 

The sexual form of E. australis is very uncommon and has been reported only in Brazil (Bitancourt & Jenkins, 1936, 1937). Stromata contain numerous spherical asci, each harboring eight filamentous hyaline ascospores (Holliday, 1980). There is no information available on the role played by the ascospores in the disease propagation.

E. australis is able to survive in scab pustules on fruits remaining on the tree (Chung, 2011), providing the inoculum for the next season. Even in resistant cultivars, the fungus can survive on diseased shoots sprouting from susceptible rootstocks (Whiteside, 1988; Yamada, 1961).

Symptoms

Lesions of sweet orange scab vary with age and host plant species. Similar to symptoms caused by E. fawcettii, citrus tissues infected with E. australis show erumpent scab pustules (Chung, 2011). In contrast with E. fawcettii which affects all parts of citrus, E. australis affects mostly fruit. Fruits are infected in the early stages of their development, i.e. when not more than 20 mm across. They grow misshapen, becoming scarred and distorted, and are subject to premature fall (CABI, 2020). On the rind of developed fruits, raised lesions are formed with different shapes, sizes and colours according to the species and cultivar affected. They appear as scattered protuberances, conical projections or crater-like outgrowths, or they coalesce to give scabby patches or extensive areas of fine eruptions. Scab lesions do not extend into the albedo. E. australis forms larger, smoother, more circular scabs than E. fawcettii scabs, which are typically irregular, warty and deeply fissured.

Sweet orange scab may be confused with other diseases, e.g. bacterial canker (Xanthomonas citri pv. citri) and melanose (Diaporthe citri), or with injuries caused by various agents and it is difficult to differentiate it based on symptom alone (Fawcett, 1936; Brun, 1971; Knorr, 1973; Klotz, 1978; Whiteside et al., 1988).

Morphology

Ascomata pulvinate, globose, dark, pseudoparenchymatous, multilocular, up to 80-120 µm thick. Asci up to 20 per locule, subglobose or ovoid, bitunicate, inner wall thickened at the top, 12-16 µm diameter, eight-spored. Ascospores hyaline, ellipsoidal or oblong-ellipsoidal, with two to four cells, usually constricted at the central septum, 4-8 x 12-20 µm diameter. The sexual form is only known from Brazil.

Acervuli intra-epidermal or sub-epidermal, scattered or confluent, pseudoparenchymatous. Conidiogenous cells originated from the upper cells of the pseudoparenchyma or from the hyaline or pale-brown phialidic conidiophores, which have 2-4 septa. Conidia hyaline, unicellular, ellipsoid, biguttulate, 5-10 x 2-5 µm. Mycelium hyaline, scanty, septate, short-branched. Colonies in culture rose to purple coloured, and clearly raised above the agar surface and covered by tufts of short erect hyphae. 

Isolates of E. australis grow slowly in culture, lack extensive aerial hyphae and often produce red or brown pigments (Sivanesan & Critchett, 1974a, b, c). 

Detection and inspection methods

Other pathogens of citrus cause lesions similar to those of citrus scab, therefore, detection of E. australis cannot be based solely on the visual observation of symptoms. Isolation of the fungus is very challenging; but semi-selective media containing antibiotics and fungicides (dodine) have been developed to successfully isolate E. australis from scab lesions (Whiteside, 1988). For species separation, Timmer et al. (1996) found out that it is not possible to distinguish Elsinoë species by cultural characteristics such as conidial size and shape and colony colour, and they are more reliably differentiated by pathogenicity. Pathogenicity tests have been implemented for species and pathotype identification (Timmer et al., 1996; Tan et al.,1996). In addition, E. australis can be pathologically separated from E. fawcettii by its inability to infect citrus leaves. The possibility of using immunochemical methods for pathogen detection has been also envisaged (Peláez Abellán et al., 1986).

For molecular methods, a PCR test based on random amplified polymorphic DNA (RAPD) of ITS sequences has been used for differentiating E. australis from E. fawcettii (Tanh et al.,1996) and partially resolved E. australis pathotypes (Hyun et al., 2009). In addition, specific primers have been designed and successfully used for detecting both species individually. The PCR tests are effective for either fungal cultures or infected plant tissues. Combined analysis of several genetic loci is more effective for distinguishing Elsinoë species causing citrus scab (Hyun et al., 2009; Fan et al., 2017). Sequence analysis of the internal transcribed spacer (ITS) region and the translation elongation factor 1 α (TEF) gene clearly distinguished isolates of E. fawcettii and E. australis, and provided fixed nucleotide differences that distinguished subgroups separated by RAPD-PCR within the two species. Fan et al. (2017) employed combined analyses of ITS, LSU, rpb2 and TEF1-α DNA to refine the phylogeny and taxonomy of Elsinoë with descriptions of new species based on isolates originally identified as causal agents of citrus scab.

Validated international protocols for detection and characterization of E. fawcettii are currently not available

The international trade of citrus fruits, originating in infested countries, may favour long-distance movement of E. australis. Local and short-distance dissemination of the pathogen in orchards is mostly via rain (or irrigation water), although insects and, to a certain extent, wind-carried water droplets containing spores may contribute to the spread.

Economic impact

E. australis is economically more significant than E. fawcettii as it attacks all sweet orange cultivars as well as some tangerines and their hybrids which are widely grown. Severely infected fruits are scarred and distorted, and consequently unmarketable. 

Citrus scab is important only in areas where susceptible species or cultivars of citrus fruit are grown for the fresh market and where young plants or new growth develops under favourable conditions of temperature, moisture and shade (CABI, 2020). Losses largely depend on seasonal and local weather conditions and impact may be extremely reduced in areas with a limited annual rainfall of less than 1300 mm.

Control

Scab disease caused by E. australis can be controlled both in the nursery and in the orchard by agricultural practices, sanitation, chemical treatments. Management measures may include the use of resistant citrus cultivars (Ieki, 1982; Yoshida & Shichijo, 1984; Reddy et al., 1986), as well as adequate tree spacing, row orientation and pruning in order to improve ventilation within the orchard. Sanitation measures represent the most effective strategy for scab management and aim to eliminate inoculum sources of E. australis, through removal of symptomatic fruits and even destruction of all diseased trees. In countries where the disease occurs, chemical control is widely used and several synthetic fungicides such as benomyl, thiophanate methyl, azoxystrobin, trifloxystrobin, pyraclostrobin, ferbam, as well as copper compounds have been proven effective. When using copper in preventive treatments several sprays are needed as the entire fruit surface must be continuously covered by a copper layer during the susceptible stage (Gopal et al., 2014). However, sustainability of chemical control requires the use of appropriate fungicide spray programmes to avoid the development of resistance (González, 1980; Rao, 1983; Reddy et al., 1983). For example, benomyl-tolerant strains of the pathogen have been found (Whiteside, 1980). 

Phytosanitary risk

The import of citrus fruits from countries where the pathogen is present may present a risk of introduction of E. australis into the citrus-growing areas of the EPPO region. Citrus plants, the main hosts of E. australis, are cultivated on a vast area around the Mediterranean Basin. It has been considered that the conditions prevailing in most citrus-growing areas of the EPPO region were favourable to the establishment of E. australis (EFSA, 2017). Additionally, the prevailing climate in these citrus-growing areas combined to the practice of sprinkle and micro-sprinkle irrigation might create climatic conditions suitable to the establishment of E. australis (EFSA, 2017). Once established, the pest is highly likely to spread naturally or by means of human assistance.

As the main pathway is the movement of infected citrus fruit, restrictions on fruit trade are usually implemented in the EPPO region. It can be requested that fruit should originate from pest-free areas or from pest-free places of production as demonstrated by crop inspections and laboratory testing prior to export.

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This datasheet was extensively revised in 2020 by Clovis Douanla-Meli. His valuable contribution is gratefully acknowledged.

EPPO (2024) Elsinoë australis. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-04-18)

This datasheet was first published in the second edition of CABI/EPPO 'Quarantine Pests for Europe' in 1997 and revised in 2020. 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 (1997) Quarantine Pests for Europe (2^nd edition). CABI, Wallingford (GB).