How could pathogen transfer affect local agriculture?

by Maria Chiara Rosace, Antonino Napoleone | June 30, 2022.

Edited by Ivy Rose Sebastian.

Due to the international trade of agricultural products, there is always a latent risk of inadvertently transferring pathogens, which could lead to certain outbreaks that could affect the local agriculture.
Citrus black spot is a disease that causes considerable economic trouble for global agriculture. Fortunately, it has not yet been detected in Europe but, due to such trade activities, the causative fungus, known as Phyllosticta citricarpa, could be a potential threat in the near future. The infections caused may remain latent for prolonged periods and symptoms may appear after some time, e.g., on the fruit during transport or storage.

P. citricarpa is a pathogen for plants of the Citrus genus, especially lemon, grapefruit, mandarin, and orange. What about bergamot? What would be the consequences if this fungus arrived in Calabria, the exclusive land to produce this priceless citrus fruit? ( Read more: “Health and nutrition: can tropical fruits become local specialties?”)

Phyllosticta citricarpa: distribution

Citrus black spot was first recorded in Australia in 1895 on orange (Benson, 1895) and since then, findings have mainly covered only the southern hemisphere (Figure 1). In 2019, its presence was officially confirmed in the Mediterranean basin, in Tunisia where substantial phytosanitary measures to control the disease are underway (EPPO, online).

Phyllosticta citricarpa: biological life cycle

Phyllosticta citricarpa has two infection cycles:

• a primary cycle driven by ascospores (sexual reproduction) in the leaf litter;
• a secondary cycle involving pycnidiospores (asexual reproduction) produced on fruits, twigs, and leaf lesions (EFSA, 2021; Guarnaccia et al., 2019).

Pseudothecia containing ascospores can develop between 40 and 180 days after leaf fall, depending on temperature and humidity conditions. The release of ascospores occurs during rainfall and occasionally during irrigation. They can also be transported by the wind for considerable distances and are the main source of disease dissemination. During germination, the ascospores penetrate the cuticle of the plant tissues, remaining dormant for extended periods. Pycnidia, on the other hand, are produced on fruit, leaves and branches and are responsible for spreading spores to other parts of the same plant or neighbouring plants (Figure 2). The individual lesions produced on the fruit may merge to form large, irregularly shaped lesions that grow rapidly to cover two-thirds of the fruit surface. They represent the most damaging symptom as they extend deep into the epicarp until they reach the fruit flesh causing early fruit drop and severe post-harvest losses (Salemi et al., online).

Phyllosticta citricarpa: epidemiology

The epidemiology of citrus black spot is influenced by the availability of inoculum, the occurrence of favourable environmental conditions for infection (temperature, rainfall), the growth stage of the tree (older trees are generally more susceptible) and the age of the fruit and leaves (Kotzé, 1981, EPPO, online).

P. citricarpa is listed as a priority pest for the European Union based on the potential economic and environmental impact that would ensue post introduction of this pathogen.

Citrus black spot and bergamot

There is no experimental or field evidence that can confirm the consequences of citrus black spot on bergamot, as the disease is currently not present in southern Italy, nor in other European countries. Despite this, it is plausible to assume that, as a species belonging to the genus Citrus, bergamot can also suffer extensive damage if affected by the fungus.
Some authors have actually used Citrus bergamia (the scientific name for bergamot) together with other Citrus samples, to assess the presence of symptoms on fruits, leaves and twigs (Guarnaccia et al., 2019). It is also known that bergamot can be counted among the host plants of other Phyllosticta species, such as Phyllosticta capitalensis (Schirmacher et al., 2019). Therefore, with the exception of sour orange (Citrus aurantium) and Tahitian lime (Citrus latifolia), all commercial citrus species and cultivars are likely to be susceptible to P. citricarpa (EFSA PLH Panel, 2014), including Citrus bergamia.

What would be the consequences of citrus black spot on bergamot?

Based on existing studies on other species of the citrus family, we can presume potential consequences. Depending on the climatic conditions that are favourable for the development of the fungal infection, symptoms may emerge on various parts of the plant: fruit, leaves, and branches.

• Fruits: due to the long incubation period, symptoms on fruits would only be visible when ripe. As known from other Citrus species (Figure 3), there are four main types of symptoms, depending on temperature and fruit maturity: (i) black spot, (ii) freckle spot, (iii) false melanosis, (iv) virulent spot. The latter is the most dangerous form of lesion that extends deep within the skin and into the flesh of the fruit. Their possible presence on bergamot cannot be confirmed.

• Leaves: symptoms on leaves are rarely observed and only in highly susceptible species such as C. limon or on poorly managed trees. However, if symptoms do appear, they begin as punctiform spots visible on both leaf surfaces and may increase in size up to 3 mm in diameter. Their presence on bergamot cannot be confirmed.
• Branches: circular and slightly sunken lesions with a brown or black margin can occasionally be found on twigs, again more commonly on more susceptible plants such as C. limon. Their possible presence on bergamot cannot be confirmed.

Conclusions

Increased controls are necessary to limit the risk of citrus black spot introduction and spread on our continent. P. citricarpa-affected fruits are not marketable due to the symptoms caused by the disease. Production losses would be inestimable, especially considering the value and rarity of crops such as bergamot. Import controls should be stricter and harmonised among all EU Member States, not only against this fungal species but also against other harmful organisms that could cause serious environmental and economic damage, with major consequences for the balance of the natural ecosystem.

References

• Benson AH (1895) Black spot of the orange. Agricultural Gazette of New South Wales 6, p 249.
• EFSA (European Food Safety Authority), (2021). Pest survey card on Phyllostica citricarpa. EFSA supporting publication 2021:EN-7105. Available online:  https://arcg.is/0C0Wr8  . Last updated: 22 Dec 2021.
• EFSA PLH Panel (EFSA Panel on Plant Health), (2014). Scientific Opinion on the risk of Phyllosticta citricarpa (Guignardia citricarpa) for the EU territory with identification and evaluation of risk reduction options. EFSA Journal 2014:12(2); 3557. doi: 10.2903/j.efsa.2014.3557.
• EPPO (online) Phyllosticta citricarpa. EPPO datasheets on pests recommended for regulation. Available online. https://gd.eppo.int/taxon/GUIGCI/datasheet.
• Kotzé JM (1981) Epidemiology and control of citrus black spot in South Africa. Plant Disease Reporter 65, 945-950.
• Guarnaccia, V., Gehrmann, T., Silva‐Junior, G. J., Fourie, P. H., Haridas, S., Vu, D., … & Crous, P. W. (2019). Phyllosticta citricarpa and sister species of global importance to Citrus. Molecular plant pathology, 20(12), 1619-1635.
• Salemi, C., Del Nista, D., Rizzo, D. (online). La macchia nera degli agrumi (Citrus Black Spot). Disponibile online: https://www.regione.toscana.it/documents/10180/13941779/La+macchia+nera+degli+agrumi+aggiornata.pdf/57e0f163-e5af-85b0-606b-84d1f911bc2f?t=1608051124533
• Schirmacher, A. M., Tomlinson, J. A., Barnes, A. V., & Barton, V. C. (2019). Species‐specific real‐time PCR for diagnosis of Phyllosticta citricarpa on Citrus species. EPPO Bulletin, 49(2), 306-313.

Copyright cover image: Jonas Janner Hamann, Universidade Federal de Santa Maria (UFSM), Bugwood.org