Fusicladium effusum
(pecan scab)

F. effusum is a fungal pathogen that causes pecan scab, which can result in severe economic losses on susceptible cultivars and resulting harm to the pecan industry in areas with high rainfall where pecan is grown. The disease develops on leaves, fruits and shoots and results in loss of photosynthetic area and reduced fruit size and quality. Pecan scab can also lead to reduced fruit set in the following year due to plant stress. Fungicides used to control pecan scab are costly. It is introduced to new areas through movement of infected host material. Despite quarantine restrictions, it is likely that human-mediated transfer has occurred between the native habitats in south-eastern USA and Mexico, and locations where pecan is grown as an exotic in South America, South Africa and New Zealand. F. effusum overwinters as stroma and conidia in lesions on shoots and fruit shucks, and the conidia are dispersed in wind and rain splash. The pathogen is a threat to all pecan-growing regions with a humid, wet environment.

Pecan scab is now widely distributed (Schubert and Braun, 2002; CABI/EPPO, 2012). The first report was from the USA (Winter, 1885), where it is believed to have originated, but the pathogen has been effectively disseminated along with its host to all areas where pecan is commercially produced and where conditions are humid and wet during the growing season. Apart from the USA, it has been reported in Mexico (Garza-Lopez et al., 1996), South America (Mendes et al., 1998; Kobyashi, 1984; Mantz et al., 2009) and South Africa (Doidge et al., 1953; Crous et al., 2000). There is a report from Canada, but this is has not been confirmed (CABI/EPPO, 2012). In the USA it occurs predominantly in the south-eastern states where weather conditions are conducive to the survival and spread of the pathogen, but Cole (1953) claimed that it has been reported in all states where pecan is grown, including the dry south-western states. Pecan scab has not been reported in Australia (Anon., 1984).

A record of F. effusum in New Zealand (Pennycook, 1989; CABI/EPPO, 2012) published in previous versions of the Compendium is invalid. The source of the record (Pennycook, 1989) is based on earlier interception or quarantine records where the imported material was destroyed and the fungus eradicated ( NZFUNGI2, 2019 ). There are no further detections from New Zealand and no evidence that F. effusum is established (Ministry for Primary Industries, New Zealand, communication to CABI, 2019).

F. effusum can be spread on living, infected host material as lesions on the leaves or stems. Infected nursery material might be used for planting in new locations, or diseased scion wood might be grafted onto rootstocks. It is not known to be seedborne. Australia does not have pecan scab, and has strict phytosanitary regulations in place that limits introductions of potentially diseased material.

The pathogen needs substantial moisture to complete its life-cycle (rain and leaf wetness), hence its significance as a problem in wet, humid, pecan-growing regions (Sparks et al., 2009). Rain is important for dispersal and production of conidia, and surface wetness lasting several hours is crucial for the infection process (Gottwald and Bertrand, 1982; Gottwald, 1985).

From an economic viewpoint pecan (Carya illinoinensis) is the most important host. The other susceptible species are wild hosts in the same genus as pecan (Carya) that occupy similar habitats in the USA (Schubert et al., 2003; http://nt.ars-grin.gov/fungaldatabases). There are reports of its occurrence on Carpinus spp., but the causal agent in now considered a separate species (Schubert et al., 2003). There is an unconfirmed report of F. effusum causing disease on Juglans regia from Brazil (Mendez et al., 1998). No other species are reported to be hosts, or susceptible to infection by F. effusum.

Genetics and Reproductive Biology

The pathogen is known only by an asexual phase, producing conidia which infect the host and cause disease. F. effusum exhibits pathogenic diversity on pecan (Demaree and Cole, 1929; Converse, 1960; Graves, 1975; Conner and Stevenson, 2004). Strains can be pathogenic on one cultivar, or perhaps a few but not on others (Conner and Stevenson, 2004) and there is a history of cultivars previously resistant to pecan scab developing the disease as the pathogen adapts to host resistance genes (Goff et al., 1996).

Epidemiology

Conidia are produced early in the spring on stromata in the previous season’s lesions on twigs and shucks (Demaree, 1924). The conidia are dispersed by wind and rain (Gottwald, 1982; Gottwald and Bertrand, 1982; Latham, 1982) and they are spread to the young leaves after bud break, and subsequently from lesions that develop on the leaves and fruit (Gottwald and Bertrand, 1982). Although wet locations or seasons are particularly prone to severe scab on susceptible cultivars, pecan grown at higher altitude has less scab in the USA (Sparks et al., 2009). The disease is polycyclic with a latent period of 7-18 days, so multiple generations can occur within a season if conditions are suitable (Gottwald and Bertrand, 1982; Turechek and Stevenson, 1998).  Optimum temperature for infection is 15-25°C, with a period of leaf wetness of <10-48 h. Foliage is most susceptible 7-21 days after emergence, becoming relatively resistant to infection when fully expanded (Gottwald and Bertrand, 1982; Turechek and Stevenson, 1998). Resistance in older leaves might be due to changes in phenolics and trichome structure on the leaf surface (Wetzstein and Sparks, 1983). Nuts are susceptible to infection throughout the season (Gottwald and Bertrand, 1983). The disease can spread throughout the canopy of the tree (Bock et al., 2013), although it is often most severe in the lower canopy. In dry areas where scab is grown under irrigation (e.g. the south-western USA) pecan scab is not an issue, even on susceptible cultivars.

Process of Infection and Host Colonization

Under ideal infection conditions, conidia germinate within 3 h of inoculation (Latham and Rushing, 1988; Rushing and Latham, 1991) and after 12 h the hyphae that originate from the aspersoria penetrate the host cuticle. The hyphae grow subcuticulary along the anticlinal walls of the epidermal cells as well as ramifying into the leaf interior through the middle lamella of adjacent epidermal cells. Hyphal growth is intercellular, and melanised, bulbous cells develop on the branches of the subcuticular hyphae by 144 h. The melanised, bulbous cells push through the cuticle and support the conidiophore of the fungus. Conidia develop by 168 h after germination. Various phylloplane chemicals can influence germination of conidia (Wood et al., 1988). But Yates et al. (1996) found little difference in germination of conidia of F. effusum on the leaves of resistant, susceptible or non-host leaves, but on resistant cultivars they observed no subcuticular development of hyphae, while on susceptible subcuticular colonization of the host occurred. Fatty acids in the fruit affected sporulation of F. effusum (Gottwald and Wood, 1984).

F. effusum will infect pecan from the seedling stage throughout the life of the tree, which can exceed 100 years in commercial orchards. The disease has been reported to infect shoots, leaves, fruit and catkins (Nolen, 1926; Demaree and Cole, 1929).

No natural enemies of F. effusum have been described.

There is no evidence that F. effusum is seedborne.

F. effusum can be detected and identified by taking a sample of spores from the symptoms and observing them under a microscope to confirm the identity of the pathogen (Schubert et al., 2003). It can also be isolated from diseased plant material and grown on a wide range of media (Barnes, 1964), but potato dextrose agar or oatmeal agar are very commonly used. The fungus is slow-growing and takes approximately 3 weeks to reach a diameter of 2.5 cm, even on preferred media. Once mature, the colony can be inspected and samples of conidia observed under a microscope to confirm the identity.

Pecan scab is relatively easily detected based on visual inspection for characteristic symptoms of the disease on the foliage, fruit and shoots of its host (Nolen, 1926; Demaree, 1924, 1928; Littrell, 1980; Goff et al., 1996). Characteristic symptoms include dark black spots of scab with a velvety appearance on the surface of the affected organ.  

This is the only species of Fusicladium known to cause disease on pecan and other species in the genus Carya. Morphologically, F. effusum bears some similarity to several other Fusicladium spp. (Schubert and Braun, 2002; Partridge and Morgan-Jones, 2003; Schubert et al., 2003) but differences in spore size, morphology, and colony growth habit can generally be used to differentiate F. effusum in culture. There are no other pathogens that infect pecan and cause the same (or very similar) symptoms.

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.

Regulatory Control

There are no specific regulatory control measures for F. effusum in the USA beyond the standard regulations pertaining to the import and export of plant material. Australia does not have the disease but has strict phytosanitary regulation on the import of material from other countries (Anon., 1984).

Cultural Control

No cultural control measures are particularly effective for managing pecan scab. However, ensuring that the trees in an orchard are adequately spaced to ensure good sunlight penetration and air-flow will help reduce the severity on susceptible cultivars (Cooper and Johnson, 1986). Planting susceptible cultivars in locations that are low-lying and wet should be avoided. Ensuring old shucks (husks) are removed from trees after harvest can also reduce sources of primary inoculum, although being a polycyclic disease this is probably of very limited value.

Biological Control

Although not strictly biological control, Bacillus mycoides is a microbial agent that is thought to induce a systemically acquired resistance response and significantly reduces the severity of pecan scab (Brenneman, 2009).

Chemical Control

Fungicides are the primary method to manage pecan scab on susceptible cultivars. The earliest fungicide used to control scab was Bordeaux mixture (Demaree, 1925; Large, 1965), which can still be used to control scab for organic production of pecans in the USA. Since the 1960s, modern fungicides have been successfully used to reduce the impact of scab (Large, 1965). In  the USA there are now several classes of fungicide that can be used including dithiocarbamates, benzimidazoles, triazoles, strobilurins, guanadines, dialkyldithiocarbamates and organometals (Hudson et al., 2012) and most recently phosphites (Bock et al., 2013), which are thought to elicit a systemically acquired resistance response. However, fungicide resistance is an issue with some of these fungicides (Litrell, 1976; Littrell and Bertrand, 1981; Reynolds et al., 1997; Stevenson, 1999; Stevenson et al., 2004; Seyran et al., 2010b). To ensure prolonged efficacy against pecan scab, either alternate sprays or mixes of fungicides with different activity are advised (Isakeit, 2010). One issue with fungicides is obtaining sufficient spray coverage in mature pecan trees, which can grow to a height of >30 m. Powerful air-blast sprayers provide disease control to a height of 10 m, but above that control of scab is diminished (Bock et al., 2013). In areas where scab is a problem aerial application of fungicide might reduce disease (Bertrand and Brenneman, 2001; Sumner, 2004; Reilly et al., 2007) and reduce the risk of fungicide resistance developing where it might otherwise be exposed to a gradient in fungicide.

Forecasting

There are two forecasting system for pecan scab. The first, AU-PECAN is based on recorded rain events and the 5-day average forecast of more rain (Brenneman et al., 1999; Bertrand and Brenneman, 2001). The second, the Pecan Scab Risk Assessment Tool is available on Pecan ipmPIPE (http://pecan.ipmpipe.org/map/scab/index.cfm) and uses weather data to estimate the accumulation of hours of relative humidity of 90% or more at an air temperature of 70 degrees Fahrenheit or above to produce an assessment of the risk of pecan scab (Broembsen et al., 1998; Payne and Smith, 2012).

Host Resistance and Tree Health

Several cultivars are resistant to scab. There is a history of the pathogen adapting to resistant cultivars, resulting in a loss of resistance (Goff et al., 1996). Current scab cultivars with excellent scab resistance in the southeastern USA include Elliott, Kanza, Curtis, Gloria Grand, Barton and Excel. Cultivars with good resistance to scab include Sumner. Cultivars that are particularly susceptible to scab and which should be avoided in scab-prone areas include Wichita, Desirable and Schley (http://www.caes.uga.edu/commodities/fruits/pecanbreeding/cultivars/scab_resistant.html; http://aggie-horticulture.tamu.edu/carya/index.htm). The genetics of resistance to scab in pecan suggests some additive gene action (Thompson and Grauke, 1994) and recent work has identified various markers (RAPDs, AFLPs and SSRs) that might be useful in helping breed for resistance using marker-assisted selection (Grauke et al., 2003; Beednagari et al., 2005). 

Tree health might influence scab susceptibility. Recent work has suggested that Ni nutrition might play a role in reducing the severity of scab on susceptible pecan (Wood et al., 2012).

Epidemiology

Although some good information exits on fundamental aspects of spore production and the environmental factors influencing it, there is little information on the spread of the pathogen and disease within or among trees. How important is inter-tree spread in epidemics? Rainfall  that results in free moisture on susceptible tissue can result in an infection cycle. With multiple wet periods numerous cycles can occur but additional information is needed on the exact parameters of rain events, temperature, humidity, and tissue growth stage influence on epidemics.How do rain events and the temperature and humidity associated with them influence epidemic development? Can further detailed information on these aspects be used to improve the existing forecasting methods?

Genetic diversity and population biology

F. effusum has been characterized as pathogenically diverse, but there is no information available on the molecular genetics or population diversity, but tools (RFLPs, SSRs etc) exist and these could be applied to provide much useful information on these aspects of the pathogen. Armed with better knowledge of the pathogen populations, resistance breeding can be improved.

Fungicide resistance

Fungicide resistance is a real management problem in some areas, and more research is needed to understand the adapting populations of F. effusum. New tools are needed to identify and monitor the fungicide resistant strains to allow appropriate management decisions.

Reproduction

No teleomorph (sexual stage) has been identified, if it exists. Confirming the existence of a teleomorph (or not) should be a priority.

Resistance breeding

Some molecular markers have been developed in pecan. However, more are needed to identify the parts of the genome and the alleles responsible for resistance (eventually for marker assisted selection, which can help speed up the process of breeding with this long-lived and slow-growing crop). Improved, reliable and uniform screening methods also need to be developed, including scab severity assessment methods.

USA: Pecan Breeding Laboratory (ARS-USDA PBL-CGRU), USDA-ARS Pecan Breeding, 10200 FM 50, Somerville, TX 77879, http://aggie-horticulture.tamu.edu/carya/index.htm

USA: South-Eastern Fruit and Tree Nut Research Laboratory (USDA-ARS-SEFTNRL), 21 Dunbar Rd., Byron, GA 31008, http://www.ars.usda.gov/Main/docs.htm?docid=5039

USA: University of Georgia College of Agricultural and Environmental Sciences, 2360 Rainwater Road, Tifton, GA 31793-5737, http://www.caes.uga.edu/commodities/fruits/pecan/

04/06/13 Original text by:

Clive H. Bock,  USDA-ARS-SEFTNRL, 21 Dunbar Rd., Byron, GA 31008, USA