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Justification for qualification based on EPPO PM 4 Standards
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NAME OF THE ORGANISM: Colletotrichum gloeosporiodes {Glomerella cingulata} (GLOMCI)

GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):

Glomerella cingulata

Pest category:

Fungi

1- Identity of the pest/Level of taxonomic listing:

Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?

Yes

Is the pest defined at the species level or lower?:

Yes

Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?

Not relevant: Fruits (including hops) sector

If necessary, please list the species:

Is it justified that the pest is listed at a taxonomic rank below species level?

Not relevant

Conclusion:

Candidate: Fruits (including hops) sector

Justification (if necessary):

It is a species complex: Colletotrichum spp. cause two different diseases in apple fruit and foliage: bitter rot and Glomerella leaf spot (GLS). GLS is restricted to subtropical and in some areas to temperate climates, whereas bitter rot is responsible for significant yield loss worldwide, particularly during the post-harvest period. Initially thought to be caused by just two species of Colletotrichum, C. acutatum and C. gloeosporioides, advances in molecular biology and sequencing techniques enabled the identification of 25 different species capable of causing bitter rot and/or GLS of apple belonging to the C. gloeosporioides species complex (CGSC), C. acutatum species complex (CASC) and C. boninense species complex (CBSC). Three species (C. gloeosporioides, C. fructicola, and C. chrysophilum) of CGSC cause both bitter rot and GLS, 18 species (6 of CGSC and 12 of CASC) only cause bitter rot, and four species (C. aenigma and C. asianum of CGSC, C. limetticola of CASC and C. karstii of CBSC) only cause GLS. These species were found to differ in their geographical distribution, environmental and host tissue preference, pathogenicity, and fungicide sensitivities (Ali / McLaughlin et al., 2024)

Differentiating species within the Colletotrichum genus is difficult, as different species of Colletotrichum produce similar symptoms on both infected apple leaves and fruit. Furthermore, cultured Colletotrichum species are often morphologically indistinguishable from one another, and the conditions in which these cultures are grown can greatly influence morphology (Adaskaveg & Hartin 1997; González et al. 2006; Gunnell and Gubler 1992). Therefore, bitter rot and GLS were originally thought to be caused only by C. gloeosporioides teleomorph (Glomerella cingulata), and C. acutatum respectively (Sutton 2014). Advances in molecular identification via multigene sequencing have allowed for greater resolution of distinct phylogenetic species within the C. acutatum and C. gloeosporioides species complexes (Damm et al. 2012; Weir et al. 2012). In addition, members of a third species complex – C. boninense – have also recently been demonstrated to cause GLS on apple cultivars (Velho et al. 2014). Thus, our knowledge of the species responsible for bitter rot and GLS has progressed rapidly in recent years, and several phylogenetic species of Colletotrichum have been observed to infect apple fruit and/or leaves (Cited from Ali / McLaughlin et al., 2024).

Glomerella cingulata should be listed as Colletotrichum gloeosporiodes (one fungus one name, see also Index Fungorum).

2 – Status in the EU:

Is this pest already a quarantine pest for the whole EU?

Presence in the EU:

List of countries (EPPO Global Database):

Conclusion:

Justification (if necessary):

HOST PLANT N°1: Pyrus (1PYUG) for the Fruits (including hops) sector.

Origin of the listing:

Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072

Plants for planting:

Plants intended for planting

3 - Is the pest already listed in a PM4 standard on the concerned host plant?

Yes

Conclusion:

Evaluation continues

Justification (if necessary):

Inspection for Glomerella cingulata recommended in EPPO Standard PM 4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. In the responses to the questionnaire, FR and NL supported deregulation respectively because of its prevalence in orchards and because it is the teleomorph stage of the non reegulated Colletotrichum gloesporiodes. Evaluation continues in regards to the taxonomy and pathway.

4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):

Conclusion:

Not candidate

Justification:

Colletotrichum gloeosporioides species complex has a very wide host range (CABI, 2021), and has been reported in apple (Ali / McLaughlin et al., 2024), pear (Liu et al., 2014) and quince (Bigot, 1960).
Colletotrichum spp. survive from one season to the next on the tree in buds, mummified apples, and colonized dead wood and cankers. Apples mummified as a result of chemical thinning and stems left on the tree are also overwintering sites, and mummified fruit on the ground can be a source of inoculum. The homothallic leaf spot isolates of C. gloeosporioides also overwinter in leaves on the orchard floor (Sutton, 2014).
The pathogen is typically waterborne, and spreads through rain-splash (Sutton 1983); conidia are dispersed by rainfall (Sutton, 2014). Ascospores are airborne and are discharged primarily during rainfall (Sutton, 2014).
Consequently, the Fruit SEWG considered that plants for planting was not a significant pathway compared to natural spread.

5 - Economic impact:

Are there documented reports of any economic impact on the host?

Justification:

Pear anthracnose, also known as “bitter rot”, “late rot”, occurred in pear-producing areas in the Dangshan region in 2008, with the infested fruits ration over 70%, resulting in serious economic loss (Liu et al., 2014).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)

Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?

Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?

Conclusion:

Justification:

6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?

Conclusion:

Justification:

Control in orchards is depending on two factors: sanitation and application of fungicides. Sanitation focusses on removal of mummified fruit, cankers, and dead wood and branches affected by fire blight is very important in managing bitter rot effectively. It is important to remove not only older shoots affected by fire blight but also those blighted during the current season because they can become colonized and serve as an inoculum source during the same growing season. Removal of diseased fruit throughout the growing season is also very helpful in reducing the rate of disease increase. Fungicides, applied on a 10- to 14-day schedule from first cover until harvest, are the most important means of control. The disease is very difficult to control once fruit are infected (Sutton, 2014).

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?

Conclusion:

Justification:

CONCLUSION ON THE STATUS:

Disqualified: plants for planting is not considered to be a significant pathway compared to natural spread.

8 - Tolerance level:

Is there a need to change the Tolerance level:

Yes

Proposed Tolerance levels:

Delisting

9 - Risk management measures:

Is there a need to change the Risk management measure:

Yes

Proposed Risk management measure:

Delisting

REFERENCES:

Adaskaveg JE & Hartin RJ (1997) Characterization of Colletotrichum acutatum isolates causing anthracnose of almond and peach in California. Phytopathology 87:979-987. doi:10.1094/PHYTO.1997.87.9.979
Ali S, Abbasi P, McLaughlin MS & Abbasi S (2024) / McLaughlin MS, Abbasi S, Abbasi PA & Ali S (2024) Apple Bitter Rot and Glomerella Leaf Spot: A Comprehensive Review of Causal Species and Their Biology, Fungicide Sensitivities, and Management Strategies. Plant Disease 2024 May 20 (ahead of print). doi: 10.1094/PDIS-03-24-0552-FE.
Bigot C (1960) Observations sur Gloeosporium fructigenum Berk, et sur deux parasites, responsables de pourritures de Pommes en cours de conservation [Observations on Glomerella cingulata and on two parasites causing rots of stored apples]. Annales des Epiphyties 11(2), 183-200.
CABI (2021) Glomerella cingulata (anthracnose). Crop Protection Compendium CABI digital library (accessed 26/Aug/2024). https://doi.org/10.1079/cabicompendium.25356
Damm U, Cannon PF, Woudenberg JHC & Crous P (2012) The Colletotrichum acutatum species complex. Studies in Mycology 73, 37-113. doi:10.3114/sim0010.
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J & Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13(4), 414-30. doi: 10.1111/j.1364-3703.2011.00783.x
Dowling M, Peres N, Villani S & Schnabel G (2020) Managing Colletotrichum on fruit crops: a complex challenge. Plant Dis. 104:2301-2316. doi.10.1094/PDIS-11-19-2378-FE
González E, Sutton TB & Correll JC (2006) Clarification of the etiology of Glomerella leaf spot and bitter rot of apple caused by Colletotrichum spp. based on morphology and genetic, molecular, and pathogenicity tests. Phytopathology 96, 982-992.
Gunnell PS & Gubler WG (1992) Taxonomy and morphology of Colletotrichum species pathogenic to strawberry. Mycologia 84, 157-165.
Liu Y, Chen Z, Qian G, Nie Y, Qiao J & Liu F (2014) Isolation and identification of Colletotrichum gloeosporioides in pears and its biological characteristics. Agricultural Science & Technology 15(20, 191-195.
Sutton TB (1983) Epidemiology of the perfect stage of Glomerella cingulate on apples. Phytopathology 73, 1179-1183.
Sutton TB (2014) Bitter rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. Pages 20-21.
Velho AC, Stadnik MJ, Casanova L, Mondino P & Alaniz S (2014) First Report of Colletotrichum karstii causing Glomerella leaf spot on apple in Santa Catarina State, Brazil. Plant Disease 98, 157. doi:10.1094/PDIS-05-13-0498-PDN.
Weir BS, Johnston PR & Damm U (2012) The Colletotrichum gloeosporioides species complex. Studies in Mycology 73, 115-180. doi:10.3114/sim0011.