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RMD-17-01: Pest Risk Management Document – Verticillium longisporum (Verticillium stripe)

August 2018


As described by the International Plant Protection Convention (IPPC), Pest Risk Analysis (PRA) includes three stages: initiation, pest risk assessment and pest risk management. Initiating the PRA process involves identifying pests and pathways of concern and defining the PRA area. Pest risk assessment provides the scientific basis for the overall management of risk. Pest risk management is the process of identifying and evaluating potential mitigation measures which may be applied to reduce the identified pest risk to acceptable levels and selecting appropriate measures.

This Risk Management Document (RMD) includes a summary of the findings of a pest risk assessment and records the pest risk management process for the identified issue. It is consistent with the principles, terminology and guidelines provided in the IPPC standards for pest risk analysis.

Table of Contents

1.0 Executive Summary

Verticillium longisporum (V. longisporum), the fungal pathogen known to cause Verticillium wilt (also known as Verticillium stripe), affects species in the Cruciferous plant family including canola and vegetable crops (broccoli, Brussels sprouts, cabbage, Chinese cabbage, and cauliflower). It has been reported to cause stem striping and premature ripening in canola, which can lead to reduced crop yields. It is present in European countries (Belgium, Czech Republic, France, Germany, Netherlands, Poland, Russia, Sweden, the United Kingdom), United States (California, Illinois), Japan, China. It was first reported in Manitoba in 2014, and in 2016 was confirmed to be present in the provinces of British Columbia (BC), Alberta (AB), Saskatchewan (SK), Ontario (ON) and Quebec (QC).

V. longisporum is a soil-borne pest that is mainly spread by movement of infested soil and crop debris. Additionally, it has been reported to move with contaminated seed harvested from heavily infested fields. The pathogen survives through resting structures called microsclerotia which can remain viable for periods of up to 10 years or more in soil or infested debris (Heale and Karapapa, 1999).

Following the first detection of the pest on a single site in Manitoba in 2014, the Canadian Food Inspection Agency (CFIA) in conjunction with provincial and industry partners, conducted a national survey of canola fields in all canola production areas of Canada in the summer and fall of 2015. The survey results have confirmed that this pest is widely distributed in most canola production areas in Canada and is present in six of the nine provinces surveyed. Based on its widespread distribution, the CFIA has determined that V. longisporum does not meet the International Plant Protection Convention (IPPC) definition of a quarantine pest. The regulation of V. longisporum under the Plant Protection Act is not warranted, nor is it cost-justifiable to implement official measures to control further introductions or domestic spread of this pest.

On farm biosecurity measures appear to be the best approach to manage and reduce further spread of V. longisporum.

2.0 Purpose

The purpose of this document is to communicate the CFIA risk management decision for Verticillium longisporum (verticillium stripe).

3.0 Scope

This RMD summarizes both the advantages and challenges associated with the regulation of this pest within Canada under the Plant Protection Act.

4.0 Definitions, Abbreviations and Acronyms

Definitions for terms used in this document can be found in the Plant Health Glossary of Terms or the IPPC Glossary of Phytosanitary Terms.

5.0 Background

V. longisporum, was detected in a canola field in Manitoba in 2014. This detection, originally made jointly by Manitoba Agriculture and Agriculture and Agri-Food Canada pathologists, and later confirmed by the CFIA, represented the first record of this disease on canola in North America. The fungus was previously known to occur in the USA, in association with cauliflower and horseradish crops.

V. longisporum primarily affects canola and other cruciferous crops. The pathogen has been present in northern Europe for several decades where it impacts winter oilseed rape production, causing leaf chlorosis and premature ripening. The disease has the potential to impact canola yields, with yield reductions highly correlated with disease severity.

As a result of the detection of V. longisporum in Manitoba, a pest risk assessment was completed by the CFIA to evaluate the risk posed by this disease to Canada's canola industry. At the time the Pest Risk Assessment (PRA) was initiated, it was unknown whether the fungus was established beyond the single confirmed site in Manitoba. Prior to the completion of the national survey, which confirmed the broad distribution of V. longisporum in Canada, the pest risk assessment had concluded that the fungus could potentially meet the definition of a quarantine pest in Canada. The fungus had the potential to cause economic harm to the Canadian canola industry, both in terms of yield losses, as well as potential trade disruptions.

The survey for V. longisporum in canola stubble took place between August and November of 2015, and was conducted by the CFIA and provincial and industry partners to determine the national distribution of the pest. This information was to be used to inform the decision of whether V. longisporum should be regulated as a quarantine pest under the Plant Protection Act.

The pest risk assessment did not evaluate the economic impacts of this disease on other cruciferous vegetable crops, nor were these production areas included in the national survey. Additional information on the impacts on cruciferous crops is included in this RMD.

6.0 Pest Risk Assessment Summary

The CFIA's pest risk assessment for V. longisporum was completed after the initial 2014 detection of the pathogen in Manitoba, in order to evaluate the potential risks to the canola industry related to the introduction of this pest into Canada. The following subsections represent the pertinent information from this assessment (Plant Health Risk Assessment Unit, 2015).

6.1 Pest Biology

V. longisporum is a vascular fungus affecting crops mainly in the family Brassicaceae. The fungus is soil-borne and spreads primarily via long-term survival structures (microsclerotia) which can remain viable in soil for many years (Heale and Karapapa, 1999). These resting bodies germinate to infect the roots of new host crops, where the fungus continues to grow into the vascular system of the plant. Later, as the plant begins to senesce near harvest, microsclerotia begin to form near harvest and continue to increase in numbers on dying and dead plant tissues (Johansson, 2006), and are returned back to the soil as the infected plant debris decays.

V. longisporum has recently been classified into three different hybrid genotypes (A1/D1, A1/D2 and A1/D3) which vary in their pathogenicity on various host crops (Depotter et al., 2016; Novakazi et al., 2015). The A1/D1 genotype has a host range including canola, cauliflower and Chinese cabbage, among others, and has previously been isolated from Europe, Japan and the USA (California). The A1/D2 genotype has only been isolated from horseradish in the USA (Illinois). The A1/D3 genotype has been reported from winter oilseed rape in Europe and Japan, but infected field grown plants are typically asymptomatic (Tran et al., 2013). While both the A1/D1 and A1/D3 genotypes have been isolated from winter oilseed rape, these two genotypes differ significantly in their pathogenicity on this crop (Tran et al., 2013).

6.2 Host Range

V. longisporum has a relatively small host range, limited primarily to Brassica species, such as canola, cabbages, bok choy, Brussels sprouts, cauliflower and broccoli. While other hosts are known from natural infections, and can show mild symptoms, economically important damage in field grown non-cruciferous crops has not been reported.

6.3 Symptoms

On canola, the onset of symptoms caused by V. longisporum occurs late in the growing season, near harvest (Dunker et al., 2006). In the field, symptoms include leaf chlorosis (particularly half-sided yellowing), development of a vertical yellow or brown stripe up one side of the stem, and early ripening. Despite its common name, wilting symptoms are not seen in canola (Depotter et al., 2016). Small black microsclerotia begin to develop within the outer layers of the dying tissues of the plant (primarily inside the stems) before harvest, giving a "peppered" appearance, and, under normal conditions, continue to develop on infested plant debris after harvest (Heale and Karapapa, 1999).

On susceptible vegetable crops, V. longisporum has been reported to cause plant wilting. Other symptoms on cauliflower and Chinese cabbage include chlorosis, stunting, defoliation and vascular discolouration (necrosis) within the stems and roots, resulting in yield reductions in the field. Cauliflower appears to be more susceptible to V. longisporum than broccoli. Crop losses in vegetable crops are mainly due to discolouration of the roots and stem tissues, rendering the plants unmarketable.

6.4 Worldwide Distribution of Verticillium longisporum

V. longisporum has been reported from several countries, including: Belgium, Czech Republic, Denmark, France, Germany, Italy, Netherlands, Poland, Russia, Sweden, United Kingdom (England and Wales), Ukraine, Japan and the USA (Illinois and California). V. longisporum has also recently been reported from Chinese cabbage in China (Yu et al., 2015). This fungus is likely more widely distributed globally than currently reported.

Results of the 2015 Canadian national survey for V. longisporum are presented in Section 7.0 Risk Management Considerations.

6.5 Pathways for Entry, Establishment and Spread

The dispersal, propagation and long-term survival of V. longisporum are mediated through the microsclerotia (Dixelius et al., 2006). Long-distance dispersal of the fungus can occur through both the movement of contaminated canola seed and the movement of farm equipment harbouring infested soil, seed or crop debris. Although there is no conclusive evidence that V. longisporum is either seed-borne or seed-transmitted in canola, it is very likely that canola seed acts as the main pathway for long-distance dispersal of the fungus into non-infested areas (Heale and Karapapa, 1999). This may occur through the contamination of canola seed or grain with microsclerotia-infested crop debris or soil during harvest, transport, cleaning or storage.

For cruciferous vegetable crops, long-distance spread of the pest is most likely to occur through trade of infected seedlings, while local spread would occur from the movement of soil contaminated farm equipment. As with canola, it is not clear whether seed is a pathway for the pest movement/spread, but other Verticillium species are known to be seed-borne on some non-cruciferous hosts.

Once established, the fungus may be readily spread naturally by wind and overland flood flows. Flooding could account for significant dispersal of the microsclerotia in those regions prone to large-scale seasonal flooding, such as southern Alberta, Saskatchewan and Manitoba.

6.6 Potential Economic and Environmental Consequences

The environmental impacts of V. longisporum were determined to be negligible.

6.6.1 Potential Economic Impacts on Canola

Prior to the completion of the national survey in 2015, and based on information of the disease on winter oilseed rape production in Europe, it had been considered that V. longisporum had significant potential to negatively impact the Canadian canola industry, both in terms of direct yield losses in the field as well as potential effects on market access. Yield reductions in winter oilseed rape appear to be highly dependent on the disease incidence in infested fields.

Crop rotation is being practiced in countries where the disease is well established and is an effective means of reducing inoculum levels in the soil to limit disease severity. For canola production, there are no effective chemical measures available to control this pathogen.

6.6.2 Potential Economic Impacts on Cruciferous Vegetable Crops

The original pest risk assessment only focused on canola and did not address the potential impacts of V. longisporum on cruciferous crop production. Further analysis of the economic impacts of the pest on these vegetable crops suggests that some crops, such as cauliflower and Chinese cabbage, can also sustain significant losses in fields where disease incidence is high. Even small amounts of inoculum can cause high levels of disease incidence in fields where susceptible cultivars are grown (Johansson, 2006; Franca et al., 2013).

In cauliflower fields, lower numbers of new microsclerotia are formed in crop debris following harvest compared to other crops such as canola (Franca et al., 2013). This may be because the harvesting of the cauliflower curd interrupts the generative phase of the crop's development and thereby restricts the spread of the fungus during the reproductive stage of plant development (Franca et al., 2013). Partially resistant cauliflower and Chinese cabbage cultivars are commercially available, and incorporation of high lignin content material, such as cauliflower, broccoli or ryegrass debris back into the soil, may also further reduce soil inoculum levels. Consequently, there are several production practices which can manage the disease in vegetable crop production systems by decreasing the number of viable V. longisporum microsclerotia present in the soil, thereby reducing the disease incidence in affected fields and decreasing direct losses due to unmarketable plants.

In addition, "Verticillium wilt" has been reported from cauliflower and Chinese cabbage fields in Manitoba and Quebec, respectively. The report from Manitoba confirmed V. dahliae, a closely related species of V. longisporum, as the causal agent, however, the report from Quebec did not identify the species of Verticillium causing the wilt symptoms. Closer investigation of these fields may show V. longisporum to be the causal agent, or to be present alongside V. dahliae, as has been observed in several other areas of the world where cauliflower and cabbages are cultivated commercially.

7.0 Risk Management Considerations

7.1 Distribution of Verticillium longisporum in Canada following the completion of the 2015 National Survey

A national survey for V. longisporum was completed in the fall of 2015 by the CFIA along with provincial and industry partners to assess the distribution of this pest in the canola production areas of Canada. A total of 1,074 fields were surveyed in nine provinces. V. longisporum was detected in six of the nine provinces surveyed (British Columbia, Alberta, Saskatchewan, Manitoba, Ontario and Quebec), which represent the major canola production regions. The pest was not detected in three of the provinces surveyed (New Brunswick, Nova Scotia and Prince Edward Island).

The novel diagnostic assay that was utilized to test all the samples collected in the survey was developed at the CFIA and was based on previous work on assays developed for both V. dahliae and V. alfalfa (Bilodeau et al., 2012). The assay is a realtime PCR based diagnostic test that is both sensitive and specific for V. longisporum and can be used directly on DNA extracted from field collected plant tissue or soil.

In total, 263 canola fields tested positive for the presence of V. longisporum DNA indicating that the fungus is widespread in western and central Canada. Further molecular analysis of select V. longisporum positive samples from Manitoba, Saskatchewan, Alberta and Ontario determined that the isolates collected from canola stubble in these provinces belonged to the A1/D1 genotype. The genotype of V. longisporum isolated from canola fields in British Columbia and Quebec was not determined.

7.2 General Risk Management Considerations

7.3 Specific Risk Management Considerations in Canola

7.4 Specific Risk Management Considerations for Cruciferous Vegetable Crops

8.0 Pest Risk Management Options

The proposed pest risk management options are primarily based on the results of the Verticillium national survey that was completed in late 2015. These results confirmed that V. longisporum is widely distributed in most canola growing areas of Canada. No country, including any of Canada's trading partners, is known to regulate V. longisporum on canola. This fact was also taken into consideration.

8.1 Pest Risk Management Option 1: Not Adding Verticillium longisporum to the List of Pests Regulated by Canada

Considerations supporting Option 1:


8.2 Pest Risk Management Option 2: Adding Verticillium longisporum to the List of Pests Regulated by Canada

Considerations Supporting Option 2:


9.0 Risk Management Decision

9.1 Consultation

Stakeholder communications were initiated shortly after the initial pest detection and resulted in the formation of the Verticillium Technical Advisory Group in June 2015. This stakeholder group included representatives from grower and industry associations from the grains and oilseeds sector, the Canola Council of Canada, provincial governments, life science companies and academic institutions, the CFIA, Agriculture and Agri-Food Canada and other federal departments or agencies.

Comments on this Pest Risk Management Document, including the CFIA's recommendation were reviewed at the conclusion of the 60 day comment period (March 15 to May 15, 2017) and discussed with the Verticillium Technical Advisory Group. The CFIA obtained broad support from stakeholders to proceed with Pest Risk Management Option 1: Not adding Verticillium longisporum to the List of Pests Regulated by Canada.

9.2 Decision

The CFIA is formally notifying that V. longisporum is widely distributed in Canada. The regulation of V. longisporum under the Plant Protection Act is not warranted, nor is it cost-justifiable to implement official measures to control further introductions or domestic spread of this pest. This decision will not require any amendments to existing plant protection directives or to the CFIA's Automated Import Reference System.

10.0 References

Bilodeau, G. J., S. T. Koike, P. Uribe and F. N. Martin. 2012. Development of an assay for rapid detection and quantification of Verticillium dahliae in soil. Phytopathology 102:331-343.

Dixelius, C., I. Happstadius and G. Berg. 2006. Verticillium wilt on Brassica oilseed crops - PDF (6517 kb). IOBC/wprs Bulletin Vol. 29(7). pp.  361-370.

Dunker, S., H. Keunecke and A. von Tiedemann. 2006. Verticillium longisporum in winter oilseed rape – Impact on plant development and yield. Integrated Control in Oilseed Crops. IOBC/wprs Bulletin Vol. 29(7). pp. 361-370.

Franca, S. C., K. Spiessens, S. Pollet, J. Debode, L. De Rooster, D. Callens and M. Höfte. 2013. Populations dynamics of Verticillium species in cauliflower fields: Influence of crop rotation, debris removal and ryegrass incorporation. Crop Protection. 54: 134-141.

Heale, J. and V. Karapapa. 1999. The Verticillium threat to Canada's major oilseed crop: canola. Canadian Journal of Plant Pathology. 21: 1-7.

Depotter, J. R. L., S. Deketelaere, P. Inderbitzin, A. von Tiedemann, M. Höfte, K. V. Subbarao, T. A. Wood and B. P. H. J. Thomma. Accepted manuscript online: 9 DEC 2015 06:22PM EST. Verticillium longisporum, the invisible threat to oilseed rape and other Brassicaceous plant hosts. Molecular Plant Pathology. DOI: 10.1111/mpp.12350

Johansson, A. 2006. Verticillium longisporum, infection, host range, prevalence and plant defence responses. Licentiate thesis Swedish University of Agricultural Sciences, Uppsala.

IPPC. 2006. International Standards for Phytosanitary Measures No. 5, Supplement No.1, Guidelines on the interpretation and application of the concept of "official control" and "not widely distributed" (2006 Edition). Secretariat of the International Plant Protection Convention, Food and Agriculture Organization of the United Nations, Rome, Italy. 345 pp.

Novakazi, F., P. Inderbitzin, G. Sandoya, R. J. Hayes, A. von Tiedemann and K. V. Subbarao. 2015. The three lineages of the diploid hybrid Verticillium longisporum differ in virulence and pathogenicity. Phytopathology "First Look" paper.

Plant Health Risk Assessment Unit. 2015. Pest Risk Assessment of Verticillium longisporum (C. Stark) Karapapa, Bainbr. & Heale, Verticillium Wilt. PRA Request: 2014-88. Plant Health Science Division, Canadian Food Inspection Agency.

Statistics Canada. February 2012. Fruit and Vegetable Production. Catalogue no. 22-003-X. page 39.

Tran, V., S. Braus-Stromeyer, C. Timpner and G. Braus. 2013. Molecular diagnosis to discriminate pathogen and apathogen species of the hybrid Verticillium longisporum on the oilseed crop Brassica napus. Applied Genetics and Molecular Biotechnology. 97: 4467-4483.

Yu S., T. Su, J. Chen, W. Wang, F. Zhang, Y. Yu, D. Zhang, X. Zhao and G. Lu. 2015. Real-time PCR as a diagnostic tool for evaluating the resistance of Chinese cabbage cultivars to Verticillium wilt. European Journal of Plant Pathology. DOI: 10.1007/s10658-015-0706-8

11.0 Endorsement

Approved by:

Chief Plant Health Officer

Signature of the Chief Plant Health Officer is required only on completion of the pest risk management process, to indicate approval of the final decision. This section is included in the RMD after stakeholder consultation has occurred and a final decision is made.

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