# Integrating science on Xanthomonadaceae for sustainable plant disease management in Europe

Joana Costa, Joël Pothier, Jens Boch, Emilio Stefani, Marie-Agnès Jacques, Vittoria Catara, Ralf Koebnik

► To cite this version:

Joana Costa, Joël Pothier, Jens Boch, Emilio Stefani, Marie-Agnès Jacques, et al. Integrating science on Xanthomonadaceae for sustainable plant disease management in Europe. Molecular Plant Pathology, 2021, 22 (12), pp.1461-1463. 10.1111/mpp.13150. hal-03521764

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Submitted on 9 Dec 2023

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# Integrating science on *Xanthomonadaceae* for sustainable plant disease management in Europe

European Cooperation in Science and Technology (COST) is a funding organization for the creation of research networks, called COST Actions, that provide networking opportunities for researchers and innovators to strengthen Europe's capacity to address scientific, technological, and societal challenges. The EuroXanth COST Action CA16107, running from March 2017 to September 2021, created a pan-European network focusing on bacteria of the family Xanthomonadaceae, including species of Xanthomonas and Xylella fastidiosa. These bacteria belong to the most devastating plant pathogens continually challenging food security. Many of these pathogens, which infect all kinds of crop plants, such as cereals, forage crops for ruminant feed, vegetables, fruits, shrubs, and trees, are listed as quarantine or regulated organisms in the EU. Consequently, their study was considered of utmost importance for the European Community and beyond.

Over the last 4 years, the EuroXanth COST Action has held several workshops, working group meetings and international conferences, and organized training schools and international exchanges for technology transfer to early-career investigators and staff from less research-intensive countries in Europe (referred to as Inclusiveness Target Countries). As major deliverables, the COST Action has compiled resources about pathogen diagnostics, tools to study genetic diversity and population structures, repertoires of pathogenicity factors, sources of host resistance, and recommendations for disease control measures. Additionally, a database on type III effectors as key pathogenicity factors in Xanthomonas is being built and a Wiki-like platform has been generated for such effectors and for plant resistance genes against xanthomonad infection in a community science approach involving more than 70 scientists from 27 countries (http://www.xanthomonas.org/dokuwiki/).

Recent reviews have addressed several aspects of the infection cycle of xanthomonads, other aspects of the pathogens' biology, such as pigment synthesis, motility, and interaction with other microbes, and advances in biocontrol. Whereas these reviews focus on certain aspects of a group of pathogens, they do not describe a pathogen in its entirety. This gap is closed by the PATHOGEN PROFILES, as published by the British Society for Plant Pathology in the journal Molecular Plant Pathology, which are unique in how they discuss a particular pathogen in detail, including its taxonomic status, life cycle, and host range. Descriptions of disease symptoms and strategies for disease management are presented and strategies for future

work are outlined. As such, PATHOGEN PROFILES are an ideal vehicle to deliver our resources to the scientific community.

Some important xanthomonads have been recently described in PATHOGEN PROFILES, such as the citrus canker agents Xanthomonas citri subspp. aurantifolii and citri, the bacterial spot pathogen of stone fruits and almond, Xanthomonas arboricola pv. pruni, and the bacterial leaf streak pathogen of cereals, Xanthomonas translucens pv. translucens (Ference et al., 2018; Garita-Cambronero et al., 2018; Sapkota et al., 2020). Another genetically related pathogen, Xylella fastidiosa, the causal agent of various economically important diseases, such as Pierce's disease of grapes (PD), citrus variegated chlorosis (CVC), and olive quick decline syndrome (OQDS), has also been covered recently (Rapicavoli et al., 2018). Moreover, this pathogen was the subject of a Focus Issue in the APS journal Phytopathology (Almeida et al., 2019).

In a series of four PATHOGEN PROFILES, we and others address several xanthomonads that are listed on the A1 and A2 lists of the European and Mediterranean Plant Protection Organization and have not been discussed recently (Figure 1). Both lists contain pathogens that are recommended to its member countries to be regulated as quarantine pests. Pests of the A1 list are absent from the EPPO region, whereas pests of the A2 list are locally present in the EPPO region. In addition, we complement this set of pathogens with a PATHOGEN PROFILE about cassava-infecting xanthomonads because of their important socioeconomic impact worldwide.

1. X. citri pv. fuscans and Xanthomonas phaseoli pv. phaseoli are the causal agents of common bacterial blight of bean (CBB), an important disease worldwide that remains difficult to control (Chen et al., 2021). These two bean pathogens belong to distinct species within the Xanthomonas genus and have undergone a dynamic evolutionary history, including the horizontal transfer of genes encoding factors probably involved in adaptation to and pathogenicity on common beans. Seed transmission is a key point of the CBB disease cycle, favouring both vertical transmission of the pathogen and worldwide distribution of the disease through global seed trade.

2. The species Xanthomonas arboricola comprises up to nine pathogens, two of which affect nut crops: pv. juglandis, the causal agent of the bacterial blight, brown apical necrosis, and the vertical oozing canker of Persian (English) walnut, and pv. corylina, the causal
<figure><img src="image_3.png" /><figcaption>FIGURE 1 Participants in the PATHOGEN PROFILES Workshop at the COST Association headquarters in Brussels, Belgium. From left to right: Jens Boch (Germany), Joana G. Vicente (UK), Fernando Tavares (Portugal), Monika Kałużna (Poland), Jan van der Wolf (Netherlands), Marie-Agnès Jacques (France), Ralf Koebnik (France), Emilio Stefani (Italy), Bart Cottyn (Belgium), Joël F. Pothier (Switzerland), and Nicolas W.G. Chen (France)</figcaption></figure>

agent of the bacterial blight of hazelnut (Kałużna et al., 2021). These two pathovars constitute the most serious threats for walnut and hazelnut trees, respectively. Recently, a new species of xanthomonads colonizing walnut trees, named *Xanthomonas euroxanthea* after our COST Action, was discovered that we will relate to the previously described pathogens of the species *X. arboricola*.

3. Bacterial spots on tomato and pepper are caused by three *Xanthomonas* species: *Xanthomonas euvesicatoria* (pvs euvesicatoria and perforans), *Xanthomonas vesicatoria*, and *Xanthomonas hortorum* pv. *gardneri* (Osdaghi et al., 2021). This group of pathogens has undergone several taxonomic revisions that are not yet generally accepted in today's literature. The key milestones in research and management of bacterial spot diseases are nicely illustrated in a century-wide timeline, which will help newcomers to the field to better grasp the older literature.

4. Cassava bacterial blight is a severe disease caused by *X. phaseoli* pv. *manihotis* (Zárate-Chaves et al., 2021). The disease is characterized by a range of symptoms that affect mainly leaves, petioles, and stems, which eventually can lead to plant death. Cassava bacterial necrosis is another disease of this crop, caused by another *Xanthomonas* species, *Xanthomonas cassavae*, that, despite being characterized by symptoms that might be similar at first sight, has an infection outcome that is not as devastating as those caused by *X. phaseoli* pv. *manihotis*.

A fifth manuscript on the *Xanthomonas hortorum* species is currently being prepared and will soon complete this series of PATHOGEN PROFILES. This species currently comprises seven pathovars of X. hortorum (pvs carotae, cynarae, gardneri, hederae, pelargonii, taraxaci, and vitians). Members of this species cause bacterial blight and bacterial spot on important crops (e.g., artichoke, carrot, lettuce, tomato), ornamentals (e.g., ivy, pelargonium), and wild plants (e.g., dandelion). Moreover, X. hortorum strains have also been isolated from nonprimary symptomatic host plants such as peony, lavender, pot marigold, and avocado. One pathovar, X. hortorum pv. gardneri, has been classified in 2015 as an EPPO

quarantine organism and as an EU-regulated nonquarantine pest since 2019.

By compiling knowledge on some of the most important xanthomonads we hope that this series of PATHOGEN PROFILES will trigger new ideas and concepts for future efforts to understand and combat these pathogens. Open communication and collaboration among scientists, extension workers, seed producers, and other stakeholders, as impressively supported by the COST Programme, will pave the way towards more durable solutions for disease management.

Joana Costa<fnref n="1" />,<fnref n="2" />

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Joël F. Pothier<fnref n="3" />

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Jens Boch<fnref n="4" />

Emilio Stefani<fnref n="5" />

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Marie-Agnès Jacques<fnref n="6" />

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Vittoria Catara<fnref n="7" />

<figure><img src="image_8.png" /></figure>

Ralf Koebnik<fnref n="8" />

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<footnote n="1">¹Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal</footnote>

<footnote n="2">²Laboratory for Phytopathology, Instituto Pedro Nunes, Coimbra, Portugal</footnote>

<footnote n="3">³Institute for Natural Resource Sciences, Environmental Genomics and Systems Biology Research Group, Zurich University of Applied Sciences, Wädenswil, Switzerland</footnote>

<footnote n="4">⁴Department of Plant Biotechnology, Institute of Plant Genetics, Leibniz Universität Hannover, Hannover, Germany</footnote>

<footnote n="5">⁵Department of Life Sciences, University of Modena and Reggio Emilia, Reggio Emilia, Italy</footnote>

<footnote n="6">⁶AGROCAMPUS-Ouest, IRHS, INRAE, Institut Agro, Univ Angers, Beaucouzé, France</footnote>

<footnote n="7">⁷Department of Agriculture, Food and Environment, University of Catania, Catania, Italy</footnote>

<footnote n="8">⁸Plant Health Institute of Montpellier, University of Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France</footnote>
<figure><img src="image_10.png" /></figure>

Correspondence

Ralf Koebnik, Plant Health Institute of Montpellier,
University of Montpellier, CIRAD, INRAE, Institut Agro, IRD,
Montpellier, France.

Email: koebnik@gmx.de, Ralf.Koebnik@ird.fr

ORCID

Joana Costa ID https://orcid.org/0000-0001-7028-2873

Joël F. Pothier ID https://orcid.org/0000-0002-9604-7780

Emilio Stefani ID https://orcid.org/0000-0002-0093-022X

Marie-Agnès Jacques ID https://orcid.org/0000-0002-1442-917X

Vittoria Catara ID https://orcid.org/0000-0001-8076-258X

Ralf Koebnik ID https://orcid.org/0000-0002-4419-0542

REFERENCES

Almeida, R.P.P., De La Fuente, L., Koebnik, R., Lopes, J.R.S., Parnell, S. & Scherm, H. (2019) Addressing the new global threat of *Xylella fastidiosa*. *Phytopathology*, 109, 172–174.

Chen, N.W.G., Ruh, M., Darrasse, A., Foucher, J., Briand, M., Costa, J. et al. (2021) Common bacterial blight of bean: a model of seed transmission and pathological convergence. *Molecular Plant Pathology*. https://doi.org/10.1111/mpp.13067

Ference, C.M., Gochez, A.M., Behlau, F., Wang, N., Graham, J.H. & Jones, J.B. (2018) Recent advances in the understanding of *Xanthomonas citri* ssp. *citri* pathogenesis and citrus canker disease management. *Molecular Plant Pathology*, 19, 1302–1318.

Garita-Cambronero, J., Palacio-Bielsa, A. & Cubero, J. (2018) *Xanthomonas arboricola* pv. *pruni*, causal agent of bacterial spot of stone fruits and almond: its genomic and phenotypic characteristics in the *X. arboricola* species context. *Molecular Plant Pathology*, 19, 2053–2065.

Kałužna, M., Fischer-Le Saux, M., Pothier, J.F., Jacques, M.A., Obradović, A., Tavares, F. et al. (2021) *Xanthomonas arboricola* pv. *juglandis* and pv. *corylina*: brothers or distant relatives? Genetic clues, epidemiology, and insights for disease management. *Molecular Plant Pathology*. https://doi.org/10.1111/mpp.13073

Osdaghi, E., Jones, J.B., Sharma, A., Goss, E.M., Abrahamian, P., Newberry, E.A. et al. (2021) A centenary for bacterial spot of tomato and pepper. *Molecular Plant Pathology*. https://doi.org/10.1111/mpp.13125

Rapicavoli, J., Ingel, B., Blanco-Ulate, B., Cantu, D. & Roper, C. (2018) *Xylella fastidiosa*: an examination of a re-emerging plant pathogen. *Molecular Plant Pathology*, 19, 786–800.

Sapkota, S., Mergoum, M. & Liu, Z. (2020) The translucens group of *Xanthomonas translucens*: complicated and important pathogens causing bacterial leaf streak on cereals. *Molecular Plant Pathology*, 21, 291–302.

Zárate-Chaves, C.A., Gómez de la Cruz, D., Verdier, V., López, C.E., Bernal, A. & Szurek, B. (2021) Cassava diseases caused by *Xanthomonas phaseoli* pv. *manihotis* and *Xanthomonas cassavae*. *Molecular Plant Pathology*. https://doi.org/10.1111/mpp.13094