| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Colletotrichum lindemuthianum (COLLLD)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
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: Vegetable seed 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: Vegetable seed sector
Justification (if necessary):
Remarks:
- It should be noted that in the pre-molecular era, Colletotrichum with cylindrical conidia on Phaseolus vulgaris was generally regarded as C. lindemuthianum. Therefore, any identifications that is not based on sequence data and the new systematics, but only on morphology, is not reliable. Since several of the references used in the RNQP summary sheet are before the epitypification/circumscription of C. lindemuthianum based on sequence data, it is not clear whether these publications all relate to C. lindemuthianum. However, there was no other option as using these studies.
- For this reason, there are doubts regarding the link between Glomerella lindemuthiana (teleomorph, sexual morph, perfect stage, rarely found in culture or nature) and Colletotrichum lindemuthianum (anamorph, asexual morph, imperfect stage). Living strains of C. lindemuthianum have never been observed to form a sexual stage, and the morphology of the asexual stage agrees with more than one species occurring on common beans (EPPO GD, 2024).
- It should be noted that in the pre-molecular era, Colletotrichum with cylindrical conidia on Phaseolus vulgaris was generally regarded as C. lindemuthianum. Therefore, any identifications that is not based on sequence data and the new systematics, but only on morphology, is not reliable. Since several of the references used in the RNQP summary sheet are before the epitypification/circumscription of C. lindemuthianum based on sequence data, it is not clear whether these publications all relate to C. lindemuthianum. However, there was no other option as using these studies.
- For this reason, there are doubts regarding the link between Glomerella lindemuthiana (teleomorph, sexual morph, perfect stage, rarely found in culture or nature) and Colletotrichum lindemuthianum (anamorph, asexual morph, imperfect stage). Living strains of C. lindemuthianum have never been observed to form a sexual stage, and the morphology of the asexual stage agrees with more than one species occurring on common beans (EPPO GD, 2024).
2 – Status in the EU:
Is this pest already a quarantine pest for the whole EU?
No
Presence in the EU:
Yes
List of countries (EPPO Global Database):
-
Conclusion:
Candidate
Justification (if necessary):
Anthracnose of Phaseolus vulgaris is distributed worldwide (e.g. North, Central, South America, Europe, Africa, Australia and Asia), occurring wherever the host plant is grown (CABI, 2021; Schwartz et al., 2005). In the EPPO region, it is reported in countries such as Austria, Azerbaijan, Bulgaria, Czech Republic, Denmark, Finland, France, Germany, Greece, Hungary, Jordan, Morocco, Poland, Romania, Russia, Slovenia, Spain, Türkiye (CABI, 2021). Colletotrichum lindemuthianum is reported (reliable reports based on DNA sequence data) in the EU on Phaseolus vulgaris in France, Germany, and the Netherlands. Reliable reports are also available for Brazil, Colombia, India, United Kingdom and the USA on P. vulgaris, Mexico on P. lunatus and Costa Rica on P. coccineus (Liu et al. 2013, Pacheco et al. 2013, Lopez-Gonzalez et al. 2017, Gupta et al. 2022).
HOST PLANT N°1: Phaseolus vulgaris (PHSVX) for the Vegetable seed sector.
Origin of the listing:
New proposal
Plants for planting:
Seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Yes
Conclusion:
Candidate
Justification:
C. lindemuthianum is particularly affecting P. vulgaris (Ansari et al., 2004). The disease can affect all aerial parts of the bean plant. When invading pods, mycelia and conidia can infect the developing seeds (CABI, 2021). Within seeds, the fungus mostly is present in the seed coat, but also can infect cotyledons and the embryo (Ravi et al., 1999; Yesuf & Sangchote, 2005), and it can survive in stored seeds for at least 5 years (Tu, 1983). The fungus survives between crops in crop residue and seed; and can be disseminated at long distances in seeds, or at distances of 3-5m in air and water (CABI, 2021; Schwartz et al., 2005). Conidia also may be dispersed within the crop by movement of insects, animals and man, especially when foliage is moist (CABI, 2021). Moderate rainfalls at frequent intervals, particularly if accompanied by wind or splashing rain, are essential for local dissemination of conidia and development of severe epidemic. Conidia that reach plant surfaces germinates under favourable conditions, the infective hypha penetrating the cuticle and epidermis (Schwartz et al., 2005). There is a direct correlation between levels of seed infection and seedling infection in the field (Marcinkowska & Borucka, 2001; Yesuf & Sangchote, 2005, 2007; Halvorson et al., 2021). Bean plants for planting, particularly seeds, is considered as a significant pathway for C. lindemuthianum.
Remark: no scientific data found on pollen transmission in the literature.
Remark: no scientific data found on pollen transmission in the literature.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Bean anthracnose affects yield, seed quality and marketability of the bean crop (CABI, 2021). It causes greater losses in temperate and subtropical zones, causing up to 100% of yield losses when contaminated seeds are planted and prolonged conditions favorable to disease development (plant infection favoured at 13-26°C, optimum at 17°C, relative humidity > 92% or free moisture required for germination, incubation and sporulation). Infected hypocotyl develops lesions (reaching 5-7 mm in older stems) or eyespots, which may be followed by rotting. Lesions appear on surface leaves and leaf veins. Lesions on pods develops into cankers. Young pods may shrivel and dry if severely infected. C. lindemuthianum is extremely variable pathogenically e.g. between isolates from South America, Central America, Europe and Africa (Schwartz et al., 2005).
Ferrante & Bisiach (1976) reports that C. lindemuthianum can completely destroy a cultivation as observed in Italy while, Munda et al. (2002) reports this fungus as disruptive on bean in Slovenia. In Bulgaria, anthracnose of bean has a sporadic character in the plain areas, but occurs annually in the mountainous areas (Kyriakov et al., 2024).
Nowadays, in countries using pathogen-free seeds and resistant varieties (e.g. France; see Measures), the fungus is reported to be rare and causing much less impact.
Ferrante & Bisiach (1976) reports that C. lindemuthianum can completely destroy a cultivation as observed in Italy while, Munda et al. (2002) reports this fungus as disruptive on bean in Slovenia. In Bulgaria, anthracnose of bean has a sporadic character in the plain areas, but occurs annually in the mountainous areas (Kyriakov et al., 2024).
Nowadays, in countries using pathogen-free seeds and resistant varieties (e.g. France; see Measures), the fungus is reported to be rare and causing much less impact.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Major
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?
No
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:
Candidate
Justification:
The fungus infects pods directly, so it affects both yield and quality.
Remark: Colletotrichum lindemuthianum has also been reported (reliable reports based on DNA sequence data) on P. coccineus and P. lunatus (see section on taxonomy). These hosts are not extensively cultivated in the EPPO region and the disease incidence on those cultivated hosts is not high.
Remark: Colletotrichum lindemuthianum has also been reported (reliable reports based on DNA sequence data) on P. coccineus and P. lunatus (see section on taxonomy). These hosts are not extensively cultivated in the EPPO region and the disease incidence on those cultivated hosts is not high.
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?
Yes
Conclusion:
Candidate
Justification:
Certain cultivars of beans are resistant to infections by specific races of C. lindemuthianum.
Seed coat infections have been managed with various chemical and biological treatments (Mohamed et al., 2014; Bardas et al., 2009; Zabot et al., 2024) and can be combined with field inspections; but several of these active substances (e.g. thiophanate methyl and benomyl) are not authorized anymore in some EPPO countries (e.g. in the EU), or not available for organic seed production. Preventive spraying with protectant or systemic fungicides has limited effectiveness (Schwartz et al., 2005).
Production of pest-free seeds in areas with dry growing seasons has been successfully used to reduce diseases losses.
In Canada an epidemic of C. lindemuthianum was brought under control by mandatory field inspections of crops grown for seed, with a zero-tolerance for anthracnose symptoms (Tu, 1988).
Rotation for 2-3 years with non-host crops, such as cereals and corn, may reduce disease severity by reducing initial inoculum levels from infested debris (Schwartz et al., 2005). Infested bean debris should be incorporated in the soil after harvest to reduce winter survival (CABI, 2021).
It is also important to restrict the activity and movement of field workers and agricultural implements in fields when the foliage is wet from rain or dew (CABI, 2021).
Seed health tests consisting of incubating more than 400 pre-treated seeds, followed by visual examination with magnification, are documented by ISTA (2024). However, Seed treatments may affect the performance of the method.
Seed coat infections have been managed with various chemical and biological treatments (Mohamed et al., 2014; Bardas et al., 2009; Zabot et al., 2024) and can be combined with field inspections; but several of these active substances (e.g. thiophanate methyl and benomyl) are not authorized anymore in some EPPO countries (e.g. in the EU), or not available for organic seed production. Preventive spraying with protectant or systemic fungicides has limited effectiveness (Schwartz et al., 2005).
Production of pest-free seeds in areas with dry growing seasons has been successfully used to reduce diseases losses.
In Canada an epidemic of C. lindemuthianum was brought under control by mandatory field inspections of crops grown for seed, with a zero-tolerance for anthracnose symptoms (Tu, 1988).
Rotation for 2-3 years with non-host crops, such as cereals and corn, may reduce disease severity by reducing initial inoculum levels from infested debris (Schwartz et al., 2005). Infested bean debris should be incorporated in the soil after harvest to reduce winter survival (CABI, 2021).
It is also important to restrict the activity and movement of field workers and agricultural implements in fields when the foliage is wet from rain or dew (CABI, 2021).
Seed health tests consisting of incubating more than 400 pre-treated seeds, followed by visual examination with magnification, are documented by ISTA (2024). However, Seed treatments may affect the performance of the method.
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Yes
Conclusion:
Candidate
Justification:
CONCLUSION ON THE STATUS:
Recommended for listing as an RNQP, based on data
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes (new regulation proposal)
Proposed Tolerance levels:
Zero tolerance approach (for all categories), based on visual examination in the field and/or seed testing (see following risk management measures).
Justification (if necessary):
Colletotrichum lindemuthianum is a major pathogen of Phaseolus vulgaris, and seeds are a major pathway for transmission. The incidence of the disease after the transmission from seeds is influenced by climatic condition. As it can spread rapidly within a field under humid and cool conditions (e.g. disease level increasing to 100%), experts considered that establishing a tolerance level higher than 0% was not appropriate.
During Stakeholders consultation, EUROSEEDS supported classification of C. lindemuthianum as an RNQP for bean seeds.
During Stakeholders consultation, EUROSEEDS supported classification of C. lindemuthianum as an RNQP for bean seeds.
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
For all categories:
(a) No symptoms of disease caused by Colletotrichum lindemuthianum have been observed in inspections at appropriate times to detect the pest during the complete cycle of vegetation of the plants at the site of production
Or
(b) the seeds have been subjected to official testing for Colletotrichum lindemuthianum on a representative sample and using appropriate methods, and have been found, in those tests, to be free from Colletotrichum lindemuthianum. Remark: When testing, the possible effect of seed treatment on testing should be taken into account (ISTA, 2024).
(a) No symptoms of disease caused by Colletotrichum lindemuthianum have been observed in inspections at appropriate times to detect the pest during the complete cycle of vegetation of the plants at the site of production
Or
(b) the seeds have been subjected to official testing for Colletotrichum lindemuthianum on a representative sample and using appropriate methods, and have been found, in those tests, to be free from Colletotrichum lindemuthianum. Remark: When testing, the possible effect of seed treatment on testing should be taken into account (ISTA, 2024).
Justification (if necessary):
Seed treatment should not be required:
- The fungus is deep-seated in the seed, therefore fungicides are not always able to reach and kill the pathogen. For instance CABI states ‘Fungicide seed treatments reduce but do not eliminate the incidence of seed-to-seedling transmission from infected seed. The pathogen harbors beneath the seed coat, meaning that obtaining satisfactory control with a seed treatment is difficult.’ This is also highlighted in a Canadian Study (https://www.agrireseau.net/Rap/documents/b02gc09.pdf). Seed treatment alone is not an option.
- Non effective non-chemical seed treatments against C. lindemuthianum are available. Organic seed production would suffer from a treatment requirement
- Seed treatment can always be used by the grower to guaranty option (a) absence of symptoms.
In Canada an epidemic of C. lindemuthianum was brought under control by mandatory field inspections of crops grown for seed, with a zero-tolerance for anthracnose symptoms (Tu, 1988), so there is scientific evidence of that being effective. Experts agreed that at least two inspections should be performed at appropriate times during the complete cycle of vegetation (in particular after pod forming). Experts were not aware of any published evidence that roguing is sufficient.
Resistant varieties reduce the risk of outbreaks but since no resistance is reported to be fully effective against all races of the fungus, this is not proposed as a risk management measure. Resistance can be used to achieve option (a) absence of symptoms.
Considering the worldwide distribution of the pest and its seed transmission, experts considered that a PFA option was difficult to apply and would provide lower guaranties.
An ISTA method (ISTA, 2024) is available for seed testing. The existing ISTA method ‘7-006: Detection of Colletotrichum lindemuthianum in Phaseolus vulgaris (bean) seed’ (https://www.seedtest.org/en/international-rules-for-seed-testing/seed-health-methods-product-1068.html), approved in 2024, has not been validated to detect C. lindemuthianum on treated seed and states that seed treatments may affect the performance of the method.
'Official' (ISPM 5) is 'Established, authorized or performed by a national plant protection organization [FAO, 1990]'. Consequently, testing may also be carried out by professional operators under official supervision.
The use of plants for planting in French bean is rare, In general, bean is sown directly in the field (no measures recommended for the ‘vegetable propagating and planting material (other than seed) sector’).
- The fungus is deep-seated in the seed, therefore fungicides are not always able to reach and kill the pathogen. For instance CABI states ‘Fungicide seed treatments reduce but do not eliminate the incidence of seed-to-seedling transmission from infected seed. The pathogen harbors beneath the seed coat, meaning that obtaining satisfactory control with a seed treatment is difficult.’ This is also highlighted in a Canadian Study (https://www.agrireseau.net/Rap/documents/b02gc09.pdf). Seed treatment alone is not an option.
- Non effective non-chemical seed treatments against C. lindemuthianum are available. Organic seed production would suffer from a treatment requirement
- Seed treatment can always be used by the grower to guaranty option (a) absence of symptoms.
In Canada an epidemic of C. lindemuthianum was brought under control by mandatory field inspections of crops grown for seed, with a zero-tolerance for anthracnose symptoms (Tu, 1988), so there is scientific evidence of that being effective. Experts agreed that at least two inspections should be performed at appropriate times during the complete cycle of vegetation (in particular after pod forming). Experts were not aware of any published evidence that roguing is sufficient.
Resistant varieties reduce the risk of outbreaks but since no resistance is reported to be fully effective against all races of the fungus, this is not proposed as a risk management measure. Resistance can be used to achieve option (a) absence of symptoms.
Considering the worldwide distribution of the pest and its seed transmission, experts considered that a PFA option was difficult to apply and would provide lower guaranties.
An ISTA method (ISTA, 2024) is available for seed testing. The existing ISTA method ‘7-006: Detection of Colletotrichum lindemuthianum in Phaseolus vulgaris (bean) seed’ (https://www.seedtest.org/en/international-rules-for-seed-testing/seed-health-methods-product-1068.html), approved in 2024, has not been validated to detect C. lindemuthianum on treated seed and states that seed treatments may affect the performance of the method.
'Official' (ISPM 5) is 'Established, authorized or performed by a national plant protection organization [FAO, 1990]'. Consequently, testing may also be carried out by professional operators under official supervision.
The use of plants for planting in French bean is rare, In general, bean is sown directly in the field (no measures recommended for the ‘vegetable propagating and planting material (other than seed) sector’).
REFERENCES:
- Ansari KI, Palacios N, Araya C, Langin T, Egan D, Doohan FM (2004) Pathogenic and genetic variability among Colletotrichum lindemuthianum isolates of different geographic origins. Plant Pathology, 53(5) 635-642.
- Atghia O (2015) Etiology of anthracnose on common bean (Phaseolus vulgaris) in northern and west northern provinces of Iran. M.Sc. thesis. University of Tehran, Iran: 204.
- Barcelos QL, Pinto JMA, Vaillancourt LJ, Souza EA (2014) Characterization of Glomerella Strains recovered from Anthracnose Lesions on Common Bean Plants in Brazil. PLoS ONE 9(3), e90910. doi:10.1371/journal.pone.0090910.
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- Zabot GF, Gaviria-Hernández V, de Farias CRJ, Zabot GL (2024) Semisynthetic compounds for controlling Colletotrichum lindemuthianum on bean seeds. Journal of Plant Protection Research 64(2), 200-208. https://doi.org/10.24425/jppr.2024.150253).