Volume 23, Issue 5 p. 597-621
Open Access

Xanthomonas hortorum – beyond gardens: Current taxonomy, genomics, and virulence repertoires

Nay C. Dia

Nay C. Dia

Environmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zurich University of Applied Sciences, Wädenswil, Switzerland

Molecular Plant Breeding, Institute of Agricultural Sciences, ETH Zurich, Zurich, Switzerland

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Lucas Morinière

Lucas Morinière

University of Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, UMR Ecologie Microbienne, Villeurbanne, France

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Bart Cottyn

Bart Cottyn

Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke, Belgium

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Eduardo Bernal

Eduardo Bernal

Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA

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Jonathan M. Jacobs

Jonathan M. Jacobs

Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA

Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA

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Ralf Koebnik

Ralf Koebnik

Plant Health Institute of Montpellier, University of Montpellier, CIRAD, INRAe, Institut Agro, IRD, Montpellier, France

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Ebrahim Osdaghi

Ebrahim Osdaghi

Department of Plant Protection, College of Agriculture, University of Tehran, Karaj, Iran

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Neha Potnis

Neha Potnis

Department of Entomology and Plant Pathology, Auburn University, Alabama, USA

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Joël F. Pothier

Corresponding Author

Joël F. Pothier

Environmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zurich University of Applied Sciences, Wädenswil, Switzerland


Joël F. Pothier, Environmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zurich University of Applied Sciences, Wädenswil, Switzerland.

Email: [email protected]

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First published: 23 January 2022
Citations: 11



Bacteria; Phylum Proteobacteria; Class Gammaproteobacteria; Order Lysobacterales (earlier synonym of Xanthomonadales); Family Lysobacteraceae (earlier synonym of Xanthomonadaceae); Genus Xanthomonas; Species X. hortorum; Pathovars: pv. carotae, pv. vitians, pv. hederae, pv. pelargonii, pv. taraxaci, pv. cynarae, and pv. gardneri.

Host range

Xanthomonas hortorum affects agricultural crops, and horticultural and wild plants. Tomato, carrot, artichoke, lettuce, pelargonium, ivy, and dandelion were originally described as the main natural hosts of the seven separate pathovars. Artificial inoculation experiments also revealed other hosts. The natural and experimental host ranges are expected to be broader than initially assumed. Additionally, several strains, yet to be assigned to a pathovar within Xhortorum, cause diseases on several other plant species such as peony, sweet wormwood, lavender, and oak-leaf hydrangea.

Epidemiology and control

X. hortorum pathovars are mainly disseminated by infected seeds (e.g., Xhortorum pvs carotae and vitians) or cuttings (e.g., Xhortorum pv. pelargonii) and can be further dispersed by wind and rain, or mechanically transferred during planting and cultivation. Global trade of plants, seeds, and other propagating material constitutes a major pathway for their introduction and spread into new geographical areas. The propagules of some pathovars (e.g., X. horturum pv. pelargonii) are spread by insect vectors, while those of others can survive in crop residues and soils, and overwinter until the following growing season (e.g., Xhortorum pvs vitians and carotae). Control measures against Xhortorum pathovars are varied and include exclusion strategies (i.e., by using certification programmes and quarantine regulations) to multiple agricultural practices such as the application of phytosanitary products. Copper-based compounds against Xhortorum are used, but the emergence of copper-tolerant strains represents a major threat for their effective management. With the current lack of efficient chemical or biological disease management strategies, host resistance appears promising, but is not without challenges. The intrastrain genetic variability within the same pathovar poses a challenge for breeding cultivars with durable resistance.

Useful websites

https://gd.eppo.int/taxon/XANTGA, https://gd.eppo.int/taxon/XANTCR, https://gd.eppo.int/taxon/XANTPE, https://www.euroxanth.eu, http://www.xanthomonas.org, http://www.xanthomonas.org/dokuwiki


The seven pathovars of Xanthomonas hortorum collectively affect 65 plant species in 15 botanical families, including agricultural crops (e.g., tomato, carrot, lettuce), horticultural plants (e.g., pelargonium), and wild plants (e.g., dandelion). This pathogen profile gives the first comprehensive summary of Xhortorum biology, including a history of its taxonomy and an account of its broad host range, and of its distribution and epidemiology, emphasizing intrapathovar differences. The genomics work done on this species is also summarized, with a special focus on pathogen–host interactions. Most previous literature on this pathogen deals with Xhortorum as a homogenous entity. This pathogen profile highlights, for each section, intrapathovar similarities and differences, thus providing a nuanced and detailed look into the complexity of Xhortorum.


The taxonomic history of the different Xhortorum pathovars is long and complex (Figure 1), like that of the genus Xanthomonas. The earliest reports of diseases caused by Xhortorum date back to the 1890s, with the reports describing bacterial leaf spot and blight disease of English ivy in 1894 in Germany (Lindau, 1894), and bacterial blight of geraniums and bacterial leaf spot of lettuce in Massachusetts, USA, in 1898 and 1907, respectively (Stone, 1907; Stone & Smith, 1898). The first proper taxonomic description of the species causing bacterial leaf spot of lettuce, referred to as Bacterium vitians (Brown, 1918), was published in 1918 (Figure 1). In the following years, B. hederae and B. pelargonii were isolated from diseased English ivy (Arnaud, 1920) and diseased geraniums (Brown, 1923), respectively. B. vitians, Bhederae, and Bpelargoni were then reclassified in the genus Phytomonas (Bergey et al., 1923; Burkholder & Guterman, 1932). Phytomonas carotae (originally proposed as “Pseudomonas carotae”) was characterized as the bacterium responsible for bacterial blight of carrot (Kendrick, 1934).

Details are in the caption following the image
The taxonomical history of Xanthomonas hortorum, outlining official taxonomical descriptions and changes, as well as first reports or suggested reclassifications of the various pathovars

Subsequently, the four species were transferred to the genus Xanthomonas as Xhederae, Xcarotae, Xpelargonii, and Xvitians (Dowson, 1943; Starr & Burkholder, 1942). Concurrently, the bacterium responsible for the bacterial blight of Russian dandelion, first reported in the USSR (Sigrianski, 1936), was designated as X. taraxaci (Niederhauser, 1943). Those five pathogens were considered to be individual Xanthomonas species until the introduction of the infrasubspecific epithet “pathovar” (Young et al., 1978), followed by the publication of the first Approved Lists in 1980 (Skerman et al., 1980). Many Xanthomonas species, including Xhederae, Xcarotae, Xpelargonii, Xvitians, and Xtaraxaci, could only be distinguished by their host range and were thus transferred as pathovars of the polytypic species Xcampestris (Young et al., 1978).

Based on DNA–DNA hybridization (DDH) (Palleroni & Bradbury, 1993; Vauterin et al., 1995), these five Xcampestris pathovars were classified as pathovars of the new species Xhortorum (Figure 1). The pathotype strain CFBP 5858T (= LMG 733T = NCPPB 939T) of Xhortorum pv. hederae was designated as the species’ type strain. The taxonomical status of “Xhortorum pv. vitians” was unclear, and two variants were distinguished: the former pathotype strain, which is nonpathogenic on lettuce, was labelled “type A”, while “Xhortorum pv. vitians”, pathogenic on lettuce, was designated as “type B”.

A group of strains causing bacterial spot of tomato and pepper (Solanum lycopersicum and Capsicum annuum) was originally named “Pseudomonas gardneri” (Šutic, 1957). Some years later, it was suggested to be part of genus Xanthomonas (Dye, 1966), but it was not formally described as X. gardneri until the beginning of the 21st century (Jones et al., 2004). The taxonomical history of the Xanthomonas strains causing bacterial spot of tomato and pepper has been thoroughly reviewed (Osdaghi et al., 2021; Potnis et al., 2015).

Strains associated with bacterial bract spot of artichoke (Cynara scolymus) were first reported in the 1950s as members of the Xanthomonas genus (Ridé, 1956), yet the official species description as X. cynarae was only provided in 2000 (Trébaol et al., 2000). Although a few phylogenetic studies demonstrated the high genetic relatedness between Xhortorum, Xcynarae, and Xgardneri (Parkinson et al., 2009; Young et al., 2008), they were only recently formally accepted as the same taxonomic entity (Morinière et al., 2020; Timilsina et al., 2019).

Genomic, phenotypic, and pathogenicity analyses were first used to prove the synonymy of Xcynarae and Xgardneri and reclassify them as pathovars of Xcynarae (Timilsina et al., 2019). In that same study, Xhortorum and Xcynarae were acknowledged to be paraphyletic species but were kept separate, based on previous wet-lab DDH results. However, only the type strain of Xhortorum was included in the 2019 study. A comprehensive analysis revisited the taxonomy of those strains, and included all type, pathotype, or representative strains of Xhortorum and Xcynarae (Morinière et al., 2020). Standard genome-to-genome comparison parameters, such as average nucleotide identity (ANI), in silico DDH (isDDH), and tetranucleotide frequencies (Tetra), between Xhortorum and Xcynarae fell into the transition zone of the species boundary (Morinière et al., 2020), a concept described previously (Richter & Rosselló-Móra, 2009; Rosselló-Móra & Amann, 2015). Phylogenetic reconstructions suggested a continuous evolution and diversification of pathovars and phenotypic data did not reveal stable diagnostic traits allowing distinction between Xcynarae and Xhortorum strains. Xcynarae was then suggested to be a later heterotypic synonym of Xhortorum and both species were combined into an extended Xhortorum species including seven pathovars (Figure 2): Xhortorum pvs hederae, pelargonii, vitians, carotae, taraxaci, cynarae, and gardneri (Morinière et al., 2020).

Details are in the caption following the image
Whole-genome phylogeny of representative Xanthomonas hortorum strains. The tree was constructed using PhyloPhlAn v. 0.40 (Segata et al., 2013) as previously described in Morinière et al. (2020)


Making a distinction between natural and experimental hosts of plant-pathogenic bacteria is important to better understand the extent of their host range (Bull & Koike, 2015). The natural host range of a pathogen consists of naturally infected plants (i.e., in nonexperimental settings), and is the criterion for pathovar identification and classification (Dye et al., 1980). The experimental host range includes plants that show symptoms after artificial inoculation. Its scope depends on the choice of plant species and of inoculation procedures. The experimental host range provides invaluable information on the pathogen's potential to adapt to new host plants (Jacques et al., 2016).

Each Xhortorum pathovar has its own natural host range and the experimental host ranges of multiple pathovars have been studied. Additionally, many unassigned strains within Xhortorum have also been isolated from multiple different plants (e.g., wheat, peony, and hydrangea). Most of the reported natural hosts of Xhortorum belong to the Geraniaceae, Araliaceae, and Asteraceae families, while most of the reported experimental hosts of the pathogen belong to Asteraceae (Table 1). Xhortorum affects more than 65 plant species in 15 botanical families, as summarized in Table 1.

TABLE 1. The natural and experimental host range of Xanthomonas hortorum pathovars and unassigned strains
X. hortorum pv. Isolated froma Host range typeb Diseasec References
Family Plant genus Plant species
carotae Apiaceae Daucus carota N BLB Kendrick (1934); Myung et al. (2014); du Toit et al. (2014)
cynarae Asteraceae Cynara scolymus N BBS Trébaol et al. (2000)
Solanaceae Capsicum annuum E NA Timilsina et al. (2019)
gardneri Asteraceae Cynara scolymus E NA Timilsina et al. (2019)
Euphorbiaceae Euphorbia heterophylla N BS Araújo et al. (2015)
Solanaceae Solanum lycopersicum N BS Jones et al. (2004); Quezado-Duval et al. (2004); Timilsina et al. (2019)
Capsicum annuum N BS Jones et al. (2004); Timilsina et al. (2019)
Solanum americanum E BS Araújo et al. (2015)
Nicandra physaloides E BS Araújo et al. (2015)
Brassicaceae Arabidopsis thaliana E NA Cândido et al. (2008)
hederae Araliaceae Hedera helix N BLS Arnaud (1920); Trantas et al. (2016)
canariensis N BLS Suzuki et al. (2002)
nepalensis (var. sinensis) N BLS Zhang et al. (2015)
rhombea E NA Suzuki et al. (2002)
colchica E NA Leyns et al. (1984)
Schefflera atinophylla N BLS Chase (1984); Norman et al. (1999); Tolba (2017)
arboricola N BLS Chase (1984); Norman et al. (1999)
Fatsia japonica N BLS Chase (1984)
Polyscias spp. N BLS Norman et al. (1999)
Plerandra elegantissima E NA Chase (1984)
pelargonii Geraniaceae Pelargonium capitatum N BB Knauss and Tammen (1964)
peltatum N BB Starr et al. (1955)
quercifolium N BB Knauss and Tammen (1964)
radens N BB Knauss and Tammen (1964)
scandens N BB Knauss and Tammen (1964)
zonale N BB Leyns et al. (1984)
× domesticum N BB Stapp (1958)
× fragrans N BB Knauss and Tammen (1964)
× hortorum N BB Starr et al. (1955)
× ignescens N BB Knauss and Tammen (1964)
Geranium maculatum N BB Stapp (1958)
pratense N BB Starr et al. (1955)
sanguineum N BB Starr et al. (1955)
sylvaticum N BB Stapp (1958)
Euphorbiaceae Euphorbia pulcherrima E NA Rockey et al. (2015)
taraxaci Taraxacum kok-saghyz N BLS Niederhauser (1943)
vitians Asteraceae Lactuca sativa N BLS Brown (1918); Morinière et al. (2020)
serriola N BLS Toussaint et al. (2012); Morinière et al. (2020)
biennis E NA Toussaint et al. (2012)
Taraxacum officinale E NA Toussaint et al. (2012); Morinière et al. (2020)
Sonchus oleraceus E NA Toussaint et al. (2012)
asper E NA Toussaint et al. (2012)
Artemisia biennis E NA Toussaint et al. (2012)
Matricaria discoidea E NA Toussaint et al. (2012)
Arctium minus E NA Toussaint et al. (2012)
Gnaphalium uliginosum E NA Toussaint et al. (2012)
Ambrosia artemisiifolia E NA Toussaint et al. (2012)
Galinsoga quadriradiata E NA Toussaint et al. (2012)
Senecio vulgaris E NA Toussaint et al. (2012)
Solanaceae Nicotiana tabacum E NA Toussaint et al. (2012)
Solanum lycopersicum E/N? BLS Sahin et al. (2003); Al-Saleh et al. (2011); Morinière et al. (2020)
Capsicum annuum E NA Sahin et al. (2003); Al-Saleh et al. (2011)
nigromaculans Arctium lappa N BLS Parkinson et al. (2009); Dehghan-Niri and Rahimian (2016)
Unassigned Asteraceae Artemisia annua N BLS Ssekiwoko et al. (2009)
Cichorium intybus N BLS Zacaroni et al. (2012)
Calendula officinalis NA NA Parkinson et al. (2009)
Lamiaceae Lavandula dentata N BLS Koike et al. (1995)
angustifolia N BLS Koike et al. (1995); Roberts and Parkinson (2014)
× intermedia N BLS Rotondo et al. (2020)
× ginginsii E NA Rotondo et al. (2020)
Oleaceae Olea europaea NA NA Young et al. (2010)
Primulaceae Primula vulgaris N BLS Nejad et al. (2012)
Hydrangeaceae Hydrangea quercifolia N BLS Cottyn et al. (2021); Uddin et al. (1996)
arborescens N BLS Cottyn et al. (2021)
Paeoniaceae Paeonia spp. N BB Oliver et al. (2012); Klass et al. (2019)
Poaceae Triticum sp. E NA Egorova et al. (2014)
Poaceae Hordeum vulgare E NA Egorova et al. (2014)
Poaceae Secale cereale E NA Egorova et al. (2014)
Poaceae Avena sativa E NA Egorova et al. (2014)
Lauraceae Persea americana NA NA Parkinson et al. (2009)
  • a To ensure consistent botanical taxonomy, plant species nomenclature was checked on the World Flora Online database (WFO, 2021).
  • b N, natural host; E, experimental host; NA, not applicable.
  • c Disease type is only mentioned in the event of a natural host. BLS, bacterial leaf spot; BBS, bacterial bract spot; BLB, bacterial leaf blight; BS, bacterial spot; BB, bacterial blight; NA, not applicable.

X. hortorum pv. hederae is primarily known as a pathogen of English ivy (Hedera helix) (Arnaud, 1920; Trantas et al., 2016), but has also been isolated from diseased plants belonging to other Hedera species (Table 1). Some Xhortorum pv. hederae strains are pathogenic on several other plants of the Araliaceae family (e.g., Schefflera spp.) in natural ecosystems (Table 1). The experimental host range of Xhortorum pv. hederae includes false aralia (Plerandra elegantissima), Japanese ivy (Hedera rhombea) (Suzuki et al., 2002), and Persian ivy (Hedera colchica) (Leyns et al., 1984), but Xhortorum strains have not been reported on those plants in natural conditions. Another Xhortorum pathovar, pv. pelargonii, naturally occurs on a wide range of plant species from the genera Geranium and Pelargonium in the Geraniaceae family (Table 1). Some strains of Xhortorum pv. pelargonii cause mild symptoms on poinsettia (Euphorbia pulcherrima) in experimental conditions (Rockey et al., 2015).

X. hortorum pv. vitians is a pathogen of cultivated lettuce (Lactuca sativa) and probably infects its closest wild relative, the prickly lettuce (Lactuca serriola) (Morinière et al., 2020; Toussaint et al., 2012). This pathovar can be pathogenic on diverse weeds from the Asteraceae family (Table 1) (Toussaint et al., 2012). In greenhouse infection tests, several strains were weakly pathogenic on tomato and two pepper cultivars (Cannuum ‘Marengo’, a sweet pepper, and Cannuum ‘Cayenne Long Slim’, a cayenne pepper) (Al-Saleh et al., 2011; Morinière et al., 2020; Sahin et al., 2003).

To our knowledge the only known hosts of Xhortorum pvs carotae and taraxaci are their respective initial hosts of isolation. Xhortorum pv. carotae is pathogenic on wild carrot (Daucus carota) and its cultivated subspecies (Dcarota subsp. sativus) (Kendrick, 1934; Myung et al., 2014; Temple et al., 2013), while Russian dandelion (Taraxacum kok-saghyz) is the only reported host of Xhortorum pv. taraxaci (Niederhauser, 1943) (Table 1).

The only recorded natural host of Xhortorum pv. cynarae is artichoke (Cynara scolymus) (Trébaol et al., 2000) and the pathogen also caused leaf spot symptoms in infiltrated Cannuum pepper leaves (Timilsina et al., 2019) (Table 1). Xhortorum pv. gardneri is one of the four xanthomonads responsible for bacterial spot of tomato and pepper, alongside Xeuvesicatoria pv. euvesicatoria, Xeuvesicatoria pv. perforans, and Xvesicatoria (Jones et al., 2004; Osdaghi et al., 2021; Potnis et al., 2015). Xhortorum pv. gardneri strains were isolated from spot symptoms on tomato and pepper (Jones et al., 2004), as well as the weed plant Euphorbia heterophylla (Araújo et al., 2015). Some Xhortorum pv. gardneri strains are pathogenic on tomato or pepper, while other strains are pathogenic on both (Potnis et al., 2015). Moreover, greenhouse inoculations with Xhortorum pv. gardneri resulted in limited necrosis on artichoke leaves (Timilsina et al., 2019), in chlorotic spots on Arabidopsis thaliana (Cândido et al., 2008), and in leaf lesions on American black nightshade (Solanum americanum) and apple of Peru (Nicandra physaloides) (Araújo et al., 2015).

Several unclassified Xhortorum strains cause disease on other plant species such as peony (Paeonia spp.) (Klass et al., 2019; Oliver et al., 2012) and sweet wormwood (Artemisia annua) (Ssekiwoko et al., 2009) (Table 1). Strains causing an unknown disease of lavender (Lavandula dentata, L. angustifolia, and L. × intermedia) were first identified as X. campestris (Koike et al., 1995), but reclassified as Xhortorum based on sequence data (Roberts & Parkinson, 2014; Rotondo et al., 2020). Strains reported as closely related to Xhortorum are sometimes unavailable in public or private strain collections, as is the case for angular leaf spot disease of oak-leaf hydrangea (Hydrangea quercifolia) observed in Georgia, USA (Uddin et al., 1996). Recently, similar strains were reported from leaf spot symptoms on hydrangea in Flemish (Belgium) nurseries (Cottyn et al., 2021). Greater burdock (Arctium lappa) is also likely to be a natural host of some unassigned Xhortorum strains (Dehghan-Niri & Rahimian, 2016).

Other studies suggesting that some strains belong to Xhortorum have not addressed Koch's postulates. As such, it is unclear whether those strains belong to the species. For example, many Xhortorum strains were isolated from seed lots of several Poaceae plants in Russia (e.g., wheat, Triticum sp.; barley, Hordeum vulgare; rye, Secale cereale; and oat, Avena sativa) (Table 1). Infiltration of bacterial suspension through leaves induced vascular or local necrotic lesions in the corresponding Poaceae species (Egorova, 2015; Egorova et al., 2014). Two multilocus sequence analysis (MLSA) studies reported that strains belonging to Xhortorum have been isolated from diseased olive (Olea europaea) (Young et al., 2010), avocado (Persea americana), and pot marigold (Calendula officinalis) (Parkinson et al., 2009) (Table 1).


The pathovars of X. hortorum can cause bacterial spot and/or bacterial blight on numerous plant species. X. hortorum pvs hederae, taraxaci, and vitians cause bacterial leaf spot on ivy (Figure 3a), dandelion (Figure 3e), and lettuce (Figure 3g), respectively. Xhortorum pvs carotae and pelargonii cause bacterial blight on carrot (Figure 3b) and geranium (Figure 3f), respectively. The symptoms of Xhortorum pv. gardneri can be observed on tomato (Figure 3c) and/or pepper (Figure 3d), depending on the strains, while Xhortorum pv. cynarae causes bacterial spot on artichoke bracts (Figure 3h). The disease symptoms caused by all these pathogens share common characteristics but also have some subtle differences.

Details are in the caption following the image
Xanthomonas hortorum pathovars on various hosts. (a) English ivy leaf infected by Xhortorum pv. hederae. Courtesy of Forestry Images and the Penn State Department of Plant Pathology & Environmental Microbiology Archives. (b) X. hortorum pv. carotae symptoms on a carrot leaf. Photograph courtesy of E-phytia and Benoît Mériaux. (c) X. hortorum pv. gardneri symptoms on pepper (cv. Early Carl Wonder) leaves, 14 days postinoculation (dpi) with Xhortorum pv. gardneri Xg965. Photograph provided by Neha Potnis. (d) Field infection of tomato plant by Xhortorum pv. gardneri. Photograph provided by Eduardo Bernal. (e) Diseased dandelion leaf 12 dpi after inoculation with Xhortorum pv. taraxaci LM 16389 (= CFBP 8644). Photograph provided by Lucas Morinière. (f) Xhortorum pv. pelargonii on geranium (Pelargonium spp.). Photograph courtesy of Forestry Images and Nancy Gregory (University of Delaware). (g) Close-up of field infection of a lettuce leaf by Xhortorum pv. vitians. Photograph provided by Lucas Morinière. (h) Infection of artichoke head by Xhortorum pv. cynarae. Photograph courtesy of Johan Van Vaerenbergh

Diseases caused by Xhortorum pathovars are characterized by round, water-soaked lesions on the abaxial surface of leaves (capitulum artichoke bracts, in the case of Xhortorum pv. cynarae) and are usually the first symptoms observed (Norman et al., 1999; Potnis et al., 2015; Pruvost et al., 2010; Ridé, 1956; Rockey et al., 2015; Schornack et al., 2008; Trébaol et al., 2000). These small water-soaked leaf spots rapidly expand to form angular necrotic lesions.

The presence of a chlorotic halo around spots or lesions is pathovar- or plant/cultivar-dependent. For example, a chlorotic halo is present around lesions caused by Xhortorum pvs pelargonii, hederae, and taraxaci, but its presence varies in angular leaf spot caused by Xhortorum pvs carotae, vitians, and gardneri (Daughtrey & Wick, 1995; Gilbertson, 2002; Myung et al., 2014; Nameth et al., 1999; Pruvost et al., 2010). In advanced infection stages, lesions and spots usually turn dark in colour (brown to black) on plant parts affected by Xhortorum pvs pelargonii, hederae, carotae, gardneri, and vitians. They can also coalesce (e.g., in the presence of Xhortorum pvs hederae, gardneri, and vitians), giving a papery appearance to leaves affected by Xhortorum pv. vitians (Bull & Koike, 2005). In final infection stages, leaves usually harden and dry and, in the case of leaves affected by Xhortorum pv. hederae, a red-purple margin might appear on their upper surface (Suzuki et al., 2002).

Some very particular leaf symptoms are associated with certain Xhortorum pathovars. For example, Xhortorum pv. pelargonii can cause leaf margin wilting and V-shaped necrotic areas, depending on the plant species and cultivar (Daughtrey & Wick, 1995). The affected areas eventually drop off, and black stem rot occurs in case of a systemic infection. When the infection expands to the roots, it results in overall wilt and gradual plant death, but no decay or soft rot is observed (Daughtrey & Benson, 2005; Manulis et al., 1994).

Furthermore, leaves are not the only plant parts affected by Xhortorum. Xhortorum pv. gardneri affects tomato fruits, on which it causes characteristic star-shaped lesions with a raised, scabby appearance (Potnis et al., 2015). On unripe tomato fruits, symptoms look like water-soaked or slightly raised pale-green spots, sometimes surrounded by greenish-white halos. On tomato sepals, symptoms consist of brown lesions, which can turn necrotic; stem lesions are narrow, elongated, and raised (Potnis et al., 2015). Xhortorum pv. hederae occasionally affects stems and petioles (Suzuki et al., 2002), and Xhortorum pv. carotae causes disease on petioles, peduncles, stems, flowers, and leaflets (Gilbertson, 2002). Lesions caused by Xhortorum pvs carotae and vitians can be V-shaped (Gilbertson, 2002; Sahin, 1997; Scott & Dung, 2020; du Toit et al., 2014).


X. hortorum includes a pathovar causing the most devastating bacterial disease of geranium (pv. pelargonii) (Manulis et al., 1994; Munnecke, 1954), an internationally regulated seedborne pathovar affecting carrot (pv. carotae) (Scott & Dung, 2020), and a pathovar reported in most lettuce-growing areas (pv. vitians) (Sahin, 1997). Furthermore, Xhortorum pv. gardneri, in addition to three other Xanthomonas spp., is a major pathogen on tomato and/or pepper (Jones et al., 2004; Osdaghi et al., 2021; Potnis et al., 2015). Diseases caused by Xhortorum pathovars have been reported in more than 40 countries across all continents except Antarctica (Figure 4), either as one-time reports or as frequent reoccurrences. One-time reports do not necessarily mean that the diseases are not recurring or currently present. Examples of frequent reoccurrences include Xhortorum pv. carotae in Canada and the USA (EPPO, 2021), Xhortorum pv. vitians in Canada and France (Morinière et al., 2020; Toussaint, 1999; Toussaint et al., 2012), and Xhortorum pv. gardneri in the USA and Brazil (Araújo et al., 2012, 2015, 2017; Potnis et al., 2015; Quezado-Duval et al., 2004), the second and sixth largest tomato producers in 2019, respectively, by gross production value (FAOSTAT, 2021).

Details are in the caption following the image
Distribution of the seven Xanthomonas hortorum pathovars. Map from the ggmap R package (Kahle et al., 2019) and data adapted from the European and Mediterranean Plant Protection Organization (EPPO). Location is an approximation based on literature available

Data on the economic impact of Xhortorum is not available for all its pathovars, as there are no reports documenting the cost of the damage caused by Xhortorum pvs cynarae, taraxaci, and hederae. When available, economic impact reports are not recent but are nonetheless informative about the scope of the importance of Xhortorum. For example, bacterial blight of geranium caused by Xhortorum pv. pelargonii is the most devastating bacterial pathogen of geranium and can lead to total geranium loss when environmental conditions are most favourable to this pathogen (Balaž et al., 2016; Manulis et al., 1994; Munnecke, 1954; Nameth et al., 1999). Most carrot seed growers in the Pacific Northwest region of the USA, an important region for US carrot seed production, consider Xhortorum pv. carotae detrimental to seed quality (Dr Jeremiah Dung, The Oregon State University, March 2021, personal communication). In Montreal, Canada, losses due to Xhortorum pv. vitians have led to complete destruction of lettuce fields (Toussaint, 1999). In Florida, USA, the pathovar caused an estimated loss of $4 million from the early to mid-1990s (Robinson et al., 2006), and also caused substantial economic losses in California and Ohio, USA (Carisse et al., 2000; Sahin, 1997). Losses due to Xhortorum pv. gardneri were estimated to cost the Midwestern US tomato-processing industry $7–8 million (Ma, 2015; Ma et al., 2011).

X. hortorum pv. gardneri is one of the four xanthomonads causing bacterial spot of tomato and pepper, and multiple reports have studied population structure shifts of those four species, especially in the USA and Brazil (Araújo et al., 2015, 2017; Egel et al., 2018; Pereira et al., 2011). In the USA, most early reported incidences of bacterial spot disease on tomato and pepper were caused by Xeuvesicatoria pv. euvesicatoria but a population shift to Xhortorum pv. gardneri has been reported in published work (Egel et al., 2018; Ma, 2015; Ma et al., 2011) and personal communications (Dr Francesca Rotondo and Dr Sally A. Miller, The Ohio State University, March 2021, personal communication). However, recent surveys for tomato and pepper bacterial spot in Brazil have shown a limited presence of Xhortorum pv. gardneri (Araújo et al., 2017).


In general, Xhortorum pathovars thrive in warm, wet, and humid environments in fields and greenhouses (Dye, 1967; Gardner & Kendrick, 1921; Kendrick, 1934; Manulis et al., 1994; Strider, 1985; du Toit et al., 2005; Toussaint, 1999). During inoculation trials, Xhortorum pv. gardneri had a higher virulence at 20°C when compared to other bacterial spot pathogens of tomato and pepper (Araújo et al., 2011), and was more prevalent than other bacterial spot xanthomonads at higher altitudes (Araújo et al., 2017). Furthermore, Xhortorum pv. vitians has an optimal infection temperature of around 23°C (Robinson et al., 2006).

The pathovars colonize the plants through natural openings (e.g., hydathodes, stomata) or wounds (Bernal & Francis, 2021; Dougherty et al., 1974; Ridé, 1956; Schwartz et al., 2017). After gaining entry, they infect the plant vascular system (Barak et al., 2002; Munnecke, 1954). Mesophyll colonization is also possible for Xhortorum pvs pelargonii (Barel et al., 2015) and vitians (authors’ unpublished data). Infections of Xhortorum pvs pelargonii and vitians can sometimes be symptomless (Barak et al., 2002; McPherson & Preece, 1978).

The two primary sources of inoculum of Xhortorum pathovars are seeds and cuttings, although they can be disseminated through other means as well (e.g., insects, rain, and irrigation water) and can survive on weeds, crop debris, or in soils. Seed is a main source of inoculum for bacterial spot and blight caused by Xhortorum pvs carotae, gardneri, and vitians (Barak et al., 2001, 2002; Kendrick, 1934; Kuan, 1985; Mtui et al., 2010; Sahin & Miller, 1997; du Toit et al., 2005, 2014). Contaminated seed, stecklings, or seedlings may initiate an epidemic in grower fields (McDonald & Linde, 2002; du Toit et al., 2005), which could result in a nonnormal pathogen distribution, as observed for Xhortorum pv. carotae populations (Scott & Dung, 2020). This can pose a challenge to the development of detection methods and durable resistant cultivars.

X. hortorum pvs hederae and pelargonii are mainly transmitted by infected cuttings (Chittaranjan & De Boer, 1997; Norman et al., 1999) because flowers such as geraniums are commonly vegetatively propagated by cuttings. Historically, propagating facilities were inadvertently responsible for distributing infected symptomless plant material (Nameth et al., 1999).

Crop residues can allow Xhortorum pvs carotae and vitians to overwinter for several months or until the following growing season (Christianson et al., 2015; Sahin et al., 2003). Xhortorum pv. carotae can persist in infected carrot foliage on soil for up to a year (Gilbertson, 2002). Xhortorum pv. vitians can survive in crop debris for up to 1 month, in both summer and winter months (Barak et al., 2001; Fayette et al., 2018). Xhortorum pvs vitians and gardneri can survive epiphytically or infect weeds, respectively (Araújo et al., 2015; Barak et al., 2001; Fayette et al., 2018). Soil or crop debris also act as an important inoculum source for X. hortorum pv. carotae, where it can survive for up to 3 months (Kendrick, 1934), and for pv. pelargonii, which can survive in soils for up to a year (Gilbertson, 2002). Survival in weeds, plant residues, and soils can serve as a secondary inoculum source in the presence of favourable hosts and environmental conditions (Gitaitis & Walcott, 2007). If bacterial populations are high, they can re-emerge from inside the plant tissue and serve as a secondary inoculum on the plant itself or on nearby hosts.

X. hortorum pvs gardneri, carotae, and vitians are also disseminated by wind or rain, or mechanically transferred during planting and cultivation (Potnis et al., 2015; du Toit et al., 2005). Xhortorum pv. carotae has been observed in aerosolized debris generated by carrot seed threshers during field operations (du Toit et al., 2005). Xhortorum pv. pelargonii can be transmitted by greenhouse whiteflies (Trialeurodes vaporariorum) (Bugbee & Anderson, 1963), and insects were noted to be vectors for Xhortorum pv. carotae but no details (insect genus or species) were given (Gilbertson, 2002).


Visual symptom assessment is the first step to detect a suspected Xhortorum infection and subsequent identification is based on pathogen isolation. Xhortorum strains are readily isolated from infected plant tissue using serial dilution plating. Growth media used can be nonselective (e.g., nutrient agar, sucrose peptone, or yeast-dextrose-calcium carbonate [YDC] agar) or semiselective (Saddler & Bradbury, 2015). Irrespective of medium type, Xhortorum colonies are yellow, mucoid, and convex (Saddler & Bradbury, 2015).

Phenotypic profiles of this species, analysed using phenotype microarrays (e.g., Biolog, OMNILOG), remain too variable to provide an accurate identification at the species level (Akhtar & Aslam, 1990; Bouzar et al., 1999; Mirik et al., 2018; Morinière et al., 2020; Myung et al., 2010; Stoyanova et al., 2014; Trébaol et al., 2000; Uddin et al., 1996). Pathovars cannot be distinguished from one another by using such phenotypic profiling as no stable, discriminative traits exist (Morinière et al., 2020; Trébaol et al., 2000). Even though pathovar classification depends on host pathogenicity (see Taxonomy update), the identification of Xhortorum pathovars should not solely rely on the host range. Indeed, some strains of this species can naturally infect hosts other than their original host of isolation (see Host range).

SDS-PAGE protein profiling and later DDHs (Stefani et al., 1994; Vauterin et al., 1991, 1995) were used to identify Xhortorum pv. vitians “type B”, revealing the existence of aberrant strains (Table 2). Even though fatty acid profiling did not provide identification among pathovars and often remains inaccurate at the species level (Barak & Gilbertson, 2003; Mirik et al., 2018; Sahin et al., 2003; Ssekiwoko et al., 2009; Uddin et al., 1996), it still distinguished between Xhortorum pv. vitians “type B” and the unusual isolates (Sahin et al., 2003). Furthermore, a panel of 16 xanthomonad-specific monoclonal antibodies (Table 2), used in enzyme-linked immunosorbent assays (ELISAs), distinguished two serovars of Xhortorum pv. vitians isolates (Sahin et al., 2003).

TABLE 2. Non-DNA and DNA-based identification methods for Xanthomonas hortorum pathovars. The detection targets, taxonomical level of detection, and primer sequence availability, when applicable, are also reported
Detection Targeted pathovar Specific for the targeted pathovar (antibody, primer, or probe name)b Reference(s) Commentsc
method Type Target(s) Taxonomical levela
ELISA Non-DNA Polyclonal antibodies Pathovar pv. pelargonii Yes Balaž et al. (2016) Commercial ELISA kit
ELISA Non-DNA Monoclonal antibodies Xanthomonas species pv. pelargonii Yes (MAb Xpel-1) Benedict et al. (1990) NA
ELISA Non-DNA Monoclonal antibodies Pathovar pv. pelargonii Yes (McAb 2H5) Chittaranjan and De Boer (1997) NA
ELISA Non-DNA Monoclonal antibodies Xanthomonas species/pathovars pv. vitians No Sahin et al. (2003) Pattern-based discrimination
SDS-PAGE Non-DNA Various proteins Xanthomonas species/pathovars various: pvs vitians (cluster 7d), hederae (cluster 7e), pelargonii (cluster 12) No Vauterin et al. (1991) Pattern-based discrimination
SDS-PAGE Non-DNA Various proteins Xanthomonas species/pathovars pv. vitians No Stefani et al. (1994) Pattern-based discrimination
SDS-PAGE Non-DNA Various proteins Pathovar pv. gardneri No Quezado-Duval et al. (2004) Pattern-based discrimination
DDH DNA DNA homology groups Xanthomonas species/pathovars various: pvs pelargonii, hederae, vitians (group 2) No Vauterin et al. (1995) Clustering-based discrimination
MLSA/MLST DNA Various housekeeping genes, including gyrB Xanthomonas species various pvs No Parkinson et al. (2007); Young et al. (2008); Parkinson et al. (2009) Clustering-based discrimination
MLSA/MLST DNA Various housekeeping genes, including gyrB Pathovar pv. vitians No Fayette et al. (2016) Clustering-based discrimination
PCR DNA RAPD fragments Pathovar pv. carotae Yes (3S/3SR and 9B/9BR) Meng et al. (2004) D.L.: 22 fg (3S) and 2 pg (9B)
PCR DNA CDS or intergenic regions Pathovar pv. carotae Yes (XhcPP02, PP03, PP04, and PP05) Kimbrel et al. (2011) NA
PCR DNA Based on the target of XhcPP02 (Kimbrel et al., 2011) Pathovar pv. carotae Yes (Xhc-q2) Temple et al. (2013) NA
PCR DNA AFLP fragments BSX pv. gardneri Yes (Bs-XgF/Bs-XgR) Koenraadt et al. (2009); Pereira et al. (2011) NA
PCR DNA 1.2 kb DNA-fragment Pathovar pv. pelargonii Yes Manulis et al. (1994); Chittaranjan and De Boer (1997) NA
PCR DNA ERIC, REP regions Pathovar pv. pelargonii No Sulzinski et al. (1995) Pattern-based discrimination
PCR DNA ERIC fragment Pathovar pv. pelargonii Yes (XcpMl/XcpM2) Sulzinski et al. (1996); Sulzinski et al. (1997); Sulzinski et al. (1998); Sulzinski (2001) NA
PCR DNA RAPD fragments Pathovar pv. vitians Yes (B162) Barak et al. (2001) NA
PCR DNA BOXA, ERIC, REP, and 16S-23S rDNA regions Xanthomonas species/pathovars pv. vitians No Sahin et al. (2003) Pattern-based discrimination
PCR DNA SNP-based Pathovar pv. vitians No Hébert et al. (2021) Ct values
Multiplex PCR DNA ERIC fragment X. hortorum pv. pelargonii and Ralstonia solanacearum pv. pelargonii Yes (DG1/DG2) Glick et al. (2002) NA
PCR and multiplex PCR DNA AFLP fragments BSX pv. gardneri Yes (Bs-XgF/Bs-XgR) Araújo et al. (2012) D.L.: DNA: 50 pg/µl; bacterial suspension: 5 × 104 cfu/ml (100 bacterial cells per reaction).
Real-time PCR DNA ERIC fragment Pathovar pv. pelargonii Yes (XhqF/XhqR) Farahani and Taghavi (2016) D.L.: 200 fg
Multiplex real-time PCR DNA lepA BSX +Clavibacter michiganensis subsp. michiganensis, Pseudomonas syringae pv. tomato pv. gardneri No Peňázová et al. (2020) Cy5 was used for multiplex PCR that targeted BSX together
Multiplex real-time PCR DNA hrpB7 primers and probes BSX pv. gardneri Yes, in combination with probe (FP2/RP2) Strayer, Jeyaprakash, et al. (2016) D.L.: 5 × 105 cfu/ml
LAMP DNA Based on PCR product of 9B primer set (Meng et al., 2004) Pathovar pv. carotae Yes (Lace primer set) Temple and Johnson (2009); Temple et al. (2013) NA
LAMP DNA hrpB6 Pathovar pv. gardneri Yes Stehlíková et al. (2020) D.L.: 1 pg/µl
RPA DNA hrpB6 Pathovar pv. gardneri No (XGF/XGR) Strayer-Scherer et al. (2019) D.L.: 5 × 106 cfu/ml; amplified X. hortorum pv. cynarae CFBP 2044
  • a BSX, the Xanthomonas species causing bacterial spot of tomato and pepper: X. hortorum pv. gardneri, X. vesicatoria, and X. euvesicatoria pvs euvesicatoria and perforans.
  • b Primer sequences are available in all the DNA-based detection methods.
  • c D.L., reported detection limits; NA, not available.

Antibodies were used to detect Xhortorum pv. pelargonii. Pathovar-specific monoclonal antibodies (Benedict et al., 1990; Chittaranjan & De Boer, 1997) and polyclonal antibodies (Balaž et al., 2016; Mirik et al., 2018) were successfully used for serological identification of this pathogen (Table 2), using commercial double-antibody sandwich ELISA kits (LOEWE Biochemica GmbH and Agdia).

Several DNA-based molecular assays have been developed over recent decades to identify and detect Xhortorum strains (Table 2). The available methods are limited to four of the seven pathovars, as diagnostics methods are unavailable for Xhortorum pvs hederae, taraxaci, and cynarae at the time of writing. Several PCR detection protocols are available to amplify DNA from many Xanthomonas species, including one or more Xhortorum pathovars, by targeting the 16S rRNA gene (Maes, 1993), the hrp gene cluster (Leite et al., 1994), or gumD, fyuA, and the internal transcribed spacer (ITS) (Adriko et al., 2014). However, these general protocols are usually not implemented for the identification and detection of Xhortorum pathovars. Instead, targeted assays allowing specific detection and identification at the pathovar level are often preferred.

The first targeted detection DNA-based assays were mostly derived from DNA fingerprint methods, and were used to study the genetic diversity of Xhortorum pathovars (Barak & Gilbertson, 2003; Hamza et al., 2012; Sahin et al., 2003; Sulzinski, 2001). For example, a PCR for Xhortorum pv. carotae was developed from random amplified polymorphic DNA (RAPD) analysis (Meng et al., 2004). Similarly, diagnostic PCR tests for Xhortorum pv. pelargonii were developed from specific DNA fragments identified by RAPD analysis, enterobacterial repetitive intergenic consensus (ERIC) PCR or repetitive extragenic palindromic (REP) PCR (Chittaranjan & De Boer, 1997; Manulis et al., 1994; Sulzinski, 2001; Sulzinski et al., 1995, 1996, 1997, 1998). A multiplex PCR scheme for the simultaneous detection of Xhortorum pv. pelargonii and members of the Ralstonia solanacearum species complex, the second major bacterial pathogen of geranium, was developed from one of the two previously identified ERIC-PCR fragments (Glick et al., 2002). The same molecular region was used to develop a real-time quantitative PCR (qPCR) assay, allowing quantification of the pathogen (Farahani & Taghavi, 2016).

For Xhortorum pv. gardneri, a marker identified using amplified fragment polymorphism (AFLP) was initially used to design a diagnostic PCR assay (Koenraadt et al., 2009). The assay was later adapted into a multiplex PCR targeting four Xanthomonas species associated with tomato bacterial spot (Araújo et al., 2012). A multiplex TaqMan qPCR assay differentiating these four species was based on hrpB7, a less conserved gene within the hrpB operon (Strayer, Jeyaprakash, et al., 2016). A multiplex qPCR detecting these four Xanthomonas species, as well as tomato pathogens Clavibacter michiganensis subsp. michiganensis and Pseudomonas syringae pv. tomato, has been recently developed by targeting lepA (Peňázová et al., 2020).

Two Xhortorum pv. vitians-specific primer pairs, 9308B and B162, were developed from RAPD fragments (Barak et al., 2001), but their specificity to the target varied. Primer pair 9308B failed to amplify isolates recovered from lettuce and weeds around lettuce fields. On the other hand, primer pair B162 successfully detected Xhortorum pv. vitians strains isolated over a 7-year period (Barak et al., 2001).

Partial gene sequence of gyrB offers a sufficient resolution for the identification of xanthomonad isolates at the species level (Parkinson et al., 2007, 2009). MLSA is preferred to single-gene (e.g., gyrB) to outline the precise phylogeny of Xhortorum (Morinière et al., 2020). However, MLSA schemes are based on different partial gene sequences, (sub)sets of partial genes, and trimming settings, which complicates the analysis by not allowing proper comparison between studies (Catara et al., 2021). The sequencing of the first draft genome of Xhortorum pv. carotae in 2011 allowed the first use of comparative genomics to develop two new diagnostics assays to detect this pathovar (Kimbrel et al., 2011; Temple et al., 2013). The first assay used a TaqMan qPCR, whereas the second relied on loop-mediated isothermal amplification (LAMP) (Temple et al., 2013). The latter method showed superior performance compared to qPCR because of its robustness in the presence of inhibitors, and its rapidity, versatility, and usefulness in facilities with limited resources (Kimbrel et al., 2011). Both assays were also the first ones to be used as viability assays (i.e., detection of viable bacterial cells) with a xanthomonad, by including a propidium monoazide treatment prior to DNA extraction.

Two other isothermal amplification methods were recently published for the in-field detection of Xhortorum pv. gardneri (Table 2), with an emphasis on differentiation from the other xanthomonad species responsible for tomato bacterial spot. The first method is based on recombinase polymerase amplification (RPA) and targets hrcN (hrpB) (Strayer-Scherer et al., 2019). The second, based on LAMP, targets partial hrpB gene sequence (Stehlíková et al., 2020).


The genome of Xhortorum pv. gardneri ATCC 19865PT (Potnis et al., 2011) was the first Xhortorum genome publicly available in the National Center for Biotechnology Information (NCBI) database (accessed March 2021). At the time of writing, 35 Xhortorum genomes have been deposited in the database, and most (46%) were submitted in 2020 (Table 3). Their completeness varies, and 74% (n = 26) are incomplete (i.e., assembled at the scaffold or contig levels; Table 3). Eight of the nine complete Xhortorum genomes contain at least one plasmid sequence. The average genome size of Xhortorum is 5.26 Mb (4.92–5.68 Mb). The average G + C content is of 63.6% (63.2%–63.9%), and the average predicted coding sequence (CDS) number is 4260 (Table 3). The average size of Xhortorum plasmids is 86.90 kb (29.56–224.70 kb), and three plasmids in Xhortorum pvs vitians and gardneri genomes are larger than 100 kb (Table 3). The average G + C content of plasmids is 60.30% (58.07%–62.18%), with an average of 94 predicted CDS.

TABLE 3. Genome metrics of representative Xanthomonas hortorum strains
Organism Submission year Strain GenBank assembly accession Assembly level Contigs/scaffolds Size (Mb) GC (%) N50 (bp) CDSa Plasmids (bp)
X. hortorum 2017 B07-007 GCA_002285515.1 Complete 2 5.25 63.6 5,175,249 4241 pB07007 (75,655 bp)
X. hortorum 2019 VT 106 GCA_008728175.1 Complete 2 5.15 63.7 5,101,806 4135 pVT106 (44,015 bp)
X. hortorum 2020 FPH2013-1 GCA_011305375.1 Scaffold 70 5.22 63.7 190,176 4187
X. hortorum pv. carotae 2013 M081 GCA_000505565.1 Chromosome 1 5.05 63.7 5,052,399 8446
X. hortorum pv. carotae 2020 MAFF 301101 GCA_015726835.1 Contig 423 5.10 63.7 20,618 3972
X. hortorum pv. cynarae 2018 CFBP 4188PT GCA_002939985.1 Scaffold 102 5.06 63.7 145,505 4060
X. hortorum pv. cynarae 2020 CFBP 2044 GCA_903978235.1 Complete 2 5.12 63.7 5,079,002 8640 CFBP2044_p40 (40,232 bp)
X. hortorum pv. gardneri 2015 SM234-10 GCA_001009295.1 Scaffold 179 5.33 63.5 49,361 4337
X. hortorum pv. gardneri 2015 SM605-11 GCA_001009325.1 Scaffold 158 5.34 63.5 61,942 4327
X. hortorum pv. gardneri 2015 SM775-12 GCA_001009625.1 Scaffold 176 5.25 63.6 59,240 4244
X. hortorum pv. gardneri 2016 JS749-3 GCA_001908755.1 Complete 3 5.42 63.5 5,158,913 4373 pJS749-3.1 (211,336 bp), pJS749-3.2 (45,952 bp)
X. hortorum pv. gardneri 2020 CFBP 8163PT GCA_012922265.1 Contig 121 5.15 63.7 125,969 4151
X. hortorum pv. hederae 2018 CFBP 4925T GCA_002940005.1 Scaffold 313 5.32 63.8 42,684 4299
X. hortorum pv. pelargonii 2020 CFBP 2533PT GCA_012922215.1 Contig 94 5.21 63.8 134,256 4176
X. hortorum pv. taraxaci 2020 NCPPB 940PT GCA_903978185.1 Complete 2 5.03 63.8 4,999,567 8628 NCPPB940_p30 (29,567 bp)
X. hortorum pv. vitians 2020 LM 16735 GCA_012922125.1 Contig 138 5.19 63.7 118,265 4192
X. hortorum pv. vitians 2020 LMG 938neoPT GCA_012922135.1 Contig 119 5.03 63.8 141,718 4036
X. hortorum pv. vitians 2020 LM 16388 GCA_012922175.1 Contig 121 5.07 63.7 115,523 4063
X. hortorum pv. vitians 2020 CFBP 3978 GCA_012922195.1 Contig 131 5.13 63.7 141,718 4137
X. hortorum pv. vitians 2020 CFBP 499 GCA_012922335.1 Contig 132 5.17 63.7 118,955 4161
X. hortorum pv. vitians 2020 LM 16734 GCA_014338485.1 Complete 2 5.27 63.7 5,213,310 4223 pLM16734 (57,250 bp)
X. hortorum pv. vitians 2020 CFBP 498 GCA_903978195.1 Complete 4 5.68 63.2 5,365,193 4654 CFBP498_p224 (224,704 bp), CFBP498_p47 (47,063 bp), CFBP498_p41 (41,583 bp)
X. hortorum pv. vitians 2016 ICMP 7383 GCA_001908775.1 Complete 4 5.63 63.3 5,313,102 4511 pICMP7383.1 (203,385 bp), pICMP7383.2 (61,840 bp), pICMP7383.3 (47,122 bp)
  • a The number of CDS is a direct output from NCBI and three numbers appear to overestimate the actual number.

The essential genome (genes required for growth and survival, irrespective of environmental conditions; Koonin, 2000) of Xhortorum pv. vitians LM 16734 was recently characterized through saturated transposon insertion sequencing (Morinière et al., 2021) and included 370 protein-coding genes. These genes were mostly associated with critical cellular processes (e.g., translation, energy production, lipid transport), with 355 and 334 of them conserved within Xhortorum and the Xanthomonadaceae family, respectively.

8.1 Lipo- and exo-polysaccharides

Lipopolysaccharides (LPSs) are involved in biofilm formation and protecting pathogens from their environment (Corsaro et al., 2001; Newman et al., 2002, 2007). Xhortorum pv. gardneri ATCC 19865PT has a 17.7 kb ancestral-type LPS gene cluster, like that of Xcampestris pv. campestris ATCC 33913T (Potnis et al., 2011). The LPS gene clusters of Xhortorum pvs cynarae CFBP 4188PT and gardneri ATCC 19865PT were highly syntenic, but different to that of Xhortorum pv. hederae CFBP 4925T (Timilsina et al., 2019). Xhortorum pvs carotae M081, cynarae CFBP 4188PT, gardneri ATCC 19865PT, and hederae CFBP 4925T possess wzm and wzt homologs (Kimbrel et al., 2011; Potnis et al., 2011; Timilsina et al., 2019), involved in the transport of LPS band A in Pseudomonas aeruginosa (Rocchetta & Lam, 1997).

Exopolysaccharides (EPSs) are involved in xanthan biogenesis, and they protect xanthomonad pathogens from environmental stress (Kakkar et al., 2015; Kamoun & Kado, 1990; Sutherland, 1993). The EPS gene cluster of Xhortorum pvs carotae and vitians is arranged similarly to that of Xcampestris pv. campestris and contains all 12 genes from the gumB-gumM cluster (Kimbrel et al., 2011; Morinière et al., 2021). Unlike in other Xanthomonas species (Katzen et al., 1998; Kim et al., 2008), only the mutations of gumE, gumI, and gumJ were lethal in Xhortorum pv. vitians LM 16734 (Morinière et al., 2021). The presence of a tRNA gene flanking the cluster in some Xanthomonas genomes suggests a horizontal transfer acquisition (Lu et al., 2008). However, no evidence of insertion elements was found in the EPS gene cluster of Xhortorum pvs carotae and vitians (Kimbrel et al., 2011; Morinière et al., 2021).

8.2 Secretion systems

Secretion systems and their effector proteins are crucial determinants of virulence in the Xanthomonas genus (Büttner & Bonas, 2010). There are two types of type II secretion system (T2SS) clusters within Xanthomonas: the T2SS-xps, directly involved in virulence, and the T2SS-xcs, which has seemingly no direct virulence function (Szczesny et al., 2010). The pathotype strains of Xhortorum pvs hederae, gardneri, and cynarae, in addition to strain B07-007, have complete T2SS-xps (xpsD-xpsN) and T2SS-xcs (xcsC-xcsN) clusters (Alvarez-Martinez et al., 2021; Timilsina et al., 2020). Unlike T2SS-xps, the T2SS-xcs cluster is not conserved within Xanthomonas spp. (Timilsina et al., 2020) but is conserved between the four Xhortorum strains.

The type III secretion system (T3SS) delivers effector proteins that, in turn, can suppress or trigger plant defence mechanisms (Büttner, 2016; White et al., 2009). The T3SS is found in most Xanthomonas strains, including Xhortorum (Timilsina et al., 2020). The T3SS of Xhortorum pv. gardneri ATCC 19865PT is a mosaic hrp cluster, with elements like that of Xcampestris pv. campestris ATCC 33913T, but also including novel effectors (see Molecular host–pathogen interactions) (Potnis et al., 2011). Xhortorum pv. carotae M081 has a complete hrp cluster and is predicted to be functional (Kimbrel et al., 2011). Furthermore, a recent study reported that the T3SS hrp cluster in Xhortorum pv. gardneri ATCC 19865PT, cynarae CFBP 4188PT, hederae CFBP 4925T, and carotae M081 are similar, with some differences in the two 20 kb regions flanking the cluster (Merda et al., 2017).

The type IV secretion system (T4SS) is involved in protein transfer as well as bacterial conjugation (Guglielmini et al., 2014; Lawley et al., 2003; Llosa et al., 2002). Xhortorum pv. gardneri ATCC 19865PT has two plasmidborne and one chromosomal T4SS clusters (Potnis et al., 2011). The chromosomal cluster of Xhortorum pv. gardneri is complete and similar to that of Xcampestris pv. campestris ATCC 33913T. One of the two Xhortorum pv. gardneri plasmidborne clusters is 98% and 89% identical to the T4SS clusters of Burkholderia multivorans ATCC 17616 and Acidovorax avenae subsp. citrulli AAC001, respectively. The other plasmidborne cluster is similar to the one found in Xvesicatoria ATCC 35937T and Xeuvesicatoria pv. perforans 91-118 (Potnis et al., 2011). The presence of a T4SS cluster in Xhortorum pv. carotae M081 was suggested by the detection of virB genes scattered over three different contigs but its functionality was inconclusive (Kimbrel et al., 2011).

The type V secretion system (T5SS) is responsible for the secretion of various proteins, including adhesins, which are important for host colonization as they are among the first contact points between pathogen and host (Meuskens et al., 2019). The members of T5SS are autotransporters, with the exception of type 5b, which is formed of two proteins (Guérin et al., 2017). In Xanthomonas spp., T5SS clusters belong to categories 5a, 5b, and 5c (Alvarez-Martinez et al., 2021). X. hortorum pv. gardneri ATCC 19865PT and Xhortorum B07-007 have three types of T5SS (types 5a, 5b, and 5c) (Alvarez-Martinez et al., 2021).

The type VI secretion system (T6SS) is mostly responsible for bacterial antagonism, thus playing an important role in competition (Bayer-Santos et al., 2019; Russell et al., 2014). In Xanthomonas spp., three subclasses of T6SSs have been reported (T6SS-I, T6SS-II, and T6SS-III) (Alvarez-Martinez et al., 2021; Bayer-Santos et al., 2019; Timilsina et al., 2020). Xhortorum pvs hederae WHRI 7744, gardneri ATCC 19865PT, and cynarae CFBP 4188PT do not possess T6SS-I and T6SS-III clusters. A complete T6SS-II cluster was detected in Xhortorum pv. hederae WHRI 7744, but not in strains CFBP 4188PT and ATCC 19865PT (Timilsina et al., 2020). However, two different studies reported that no T6SS was found in Xhortorum pv. gardneri and Xhortorum (unspecified pathovar). In one study, strain numbers were not specified (Bayer-Santos et al., 2019), while in the other, the two strains were Xhortorum pv. gardneri ATCC 19865PT and Xhortorum B07-007 (Alvarez-Martinez et al., 2021).

8.3 Copper resistance and homeostasis

Copper resistance is attributed to the acquisition of a copper resistance gene cluster through horizontal gene transfer (Behlau et al., 2008; Bender et al., 1990; Cooksey, 1994). Copper resistance is usually plasmid encoded (Stall et al., 1986) and can thus be acquired via conjugation by other bacteria (Basim et al., 1999). Because copper-based solutions have been extensively used for controlling bacterial spot diseases, with recommendations going back to the 1920s (Abrahamian et al., 2020; Higgins, 1922; Obradovic et al., 2008), copper-resistant strains pose a challenge for disease management (see Disease control and management).

X. hortorum pv. gardneri strains differed in their response to copper. For example, strain ATCC 19865PT has copLAB homologs on the chromosome (cohLAB) and is homeostatic to copper, growing in copper concentrations up to 75 mg/L (Potnis et al., 2011). In contrast, strains JS749-3 and ICMP 7383 have plasmidborne copLAB and copMGCDF genes (Richard, Boyer, et al., 2017; Richard, Ravigné, et al., 2017), as well as cusAB/smmD systems, involved in heavy metal efflux resistance and originally described in Stenotrophomonas maltophilia (Crossman et al., 2008). Strains JS749-3 and ICMP 7383 are copper-resistant and can grow in copper concentrations up to 470 mg/L (Richard, Ravigné, et al., 2017).


The interactions of Xanthomonas species with their plant hosts involve the coordinated expression of various virulence factors (e.g., quorum sensing, effectors, avirulence genes) (Alvarez-Martinez et al., 2021; Ryan et al., 2011; Timilsina et al., 2020). Quorum sensing, a chemical communication mechanism allowing bacteria to regulate group behaviours in response to stimulus, involves the production, release, and detection of auto-inducers (Bassler, 1999; von Bodman et al., 2003; Miller & Bassler, 2001; Ng & Bassler, 2009; Whitehead et al., 2001). In Xanthomonas, the production and sensing of diffusible signal factors (DSF, e.g., α,β-unsaturated fatty acids) (Wang et al., 2004) are regulated by genes within the regulation of the pathogenicity factors (rpf) cluster.

Knocking out rpfF and rpfC in Xhortorum pv. pelargonii Xhp305 altered in planta motility, decreased disease severity on pelargonium plants, and disrupted the plant colonization pattern (Barel et al., 2015). The resulting inability of Xhortorum pv. pelargonii to switch back and forth between biofilm and planktonic lifestyles is thus DSF-dependent (Barel et al., 2015), and this shift is essential for pathogenicity (He & Zhang, 2008). Furthermore, in the rpfF and rpfC mutants, genes gumM, pilC, and pilT were down-regulated compared to the wild type, suggesting that gumM expression and biofilm production, and the type 4 pilus apparatus are DSF-dependent in Xhortorum pv. pelargonii (Barel et al., 2015).

Effectors are used by Xanthomonas species to trigger or suppress host defence mechanisms. Repertoires of effectors (effectomes) have been suggested to play a role determining host specificity (Hajri et al., 2009). Within Xhortorum, effector-related work is mainly focused on pv. gardneri, but there are also reports on pv. carotae strains (more information below). The T3SS of Xhortorum pv. gardneri ATCC 19865PT was associated with hrpW (Potnis et al., 2011), a gene predicted to encode a pectate lyase (White et al., 2009), involved in plant tissue maceration and rotting (Collmer & Keen, 1986). The function of effector gene xopZ2, located downstream of hrpW, was suggested by avrBs2 reporter gene fusion (Potnis et al., 2011). Other T3SS effectors (T3Es) in Xhortorum pv. gardneri strains were also reported: XopAM, XopAO (homolog of AvrRpm1 from P. syringae), XopAQ (homolog of Rip6/Rip11 from R. solanacearum), and XopAS (homolog of HopAS1 from Psyringae). Effectors XopAM and XopAO were demonstrated to be dependent on the T3SS using the AvrBs2 reporter system (Potnis et al., 2011). In addition, four novel T3Es were reported in multiple field strains of Xhortorum pv. gardneri: a second XopE2 paralog, in addition to XopJ and two predicted effectors, named T3EP and PTP, with homologs in Rsolanacearum and Xcampestris pv. campestris, respectively (Schwartz et al., 2015).

Effector AvrHah1, a transcription activator-like (TAL) effector of the AvrBs3/PthA family (Schornack et al., 2008), was the first characterized effector of Xhortorum pv. gardneri. AvrHah1 was able to trigger a Bs3-dependent hypersensitive response (HR) on pepper plants (Schornack et al., 2008). Gain-of-function experiments with a Xeuvesicatoria pv. euvesicatoria strain revealed that avrHah1 is responsible for enhanced water-soaking in pepper leaves, a phenotype typical for the compatible interaction of Xhortorum pv. gardneri, the donor pathogen (Schornack et al., 2008). The virulence function of AvrHah1, triggering enhanced water-soaking in its known hosts tomato, pepper, and Nicotiana benthamiana, was attributed to the movement of water into the infected apoplast (Schwartz et al., 2017). Gene avrBs7 was also identified in Xhortorum pv. gardneri as another avirulence gene as its product triggered an HR in Capsicum baccatum var. pendulum (Potnis et al., 2012). When the corresponding single dominant resistance gene Bs7 was introgressed into Cannuum ‘Early Calwonder’ (ECW), the resulting near-isogenic line ECW-70R was resistant to strains harbouring avrBs7.

Twenty-one candidate T3E genes were identified in Xhortorum pv. carotae M081, and the products of two of them, AvrBs2 and XopQ, were found to elicit effector-triggered immunity (Kimbrel et al., 2011). Using Agrobacterium-mediated transient expression of avrBs2 from Xhortorum pv. carotae in transgenic N. benthamiana triggered an HR in a Bs2-dependent manner. In contrast, no phenotypes were visible in wild-type Nbenthamiana lacking Bs2 on delivery of the same DNA construct. Transient expression of xopQ also resulted in strong and rapid HRs in most of the infiltrated leaves of wild-type Nicotiana tabacum, perhaps mediated by another resistance gene. These observations indicated a possibility for resistance gene-mediated control of Xhortorum pv. carotae (Kimbrel et al., 2011). A core Xanthomonas effectome of nine effectors, including AvrBs2, XopQ, and XopZ previously described, was reported in the tested strains of a study including Xhortorum B07-007 and Xhortorum pv. gardneri ATCC 19865PT.


An integrated control programme that focuses on excluding, reducing, or eradicating the pathogen, in combination with various methods like biological control and host resistance breeding, is the most suitable to manage bacterial spot pathogens like Xhortorum (Agrios, 2005; Marin et al., 2019). Preventing Xhortorum infections by excluding the pathogen from its hosts is crucial, especially because global trade of plants, seeds, and other propagating material plays an important role in the dissemination of this species (see Epidemiology).

Because Xhortorum pv. gardneri is locally present in the territory of the European and Mediterranean Plant Protection Organization (EPPO), the pathogen is on the EPPO A2 list and is recommended for regulation as a quarantine pest (EPPO, 2021). Since 2020, the EU (European Union) Plant Health Law regulates this pathovar as a nonquarantine pest (RNQP; Picard et al., 2018) on seeds, propagating, and planting material of tomato and peppers as well as propagating material of ornamental peppers (EU Commission, 2019). Other Regional Plant Protection Organizations (RPPOs) can implement regional phytosanitary regulations. For example, Xhortorum pv. carotae is considered an A1 plant pest by the Caribbean Plant Protection Commission (CPPC) and is under strict quarantine control there. Certification programmes propose requirements for production of disease-free plants. For example, certification scheme EPPO PM4/3 outlines various testing methods for Xhortorum pv. pelargonii on different propagation materials (nuclear, basic stock, and certified cuttings). Because cool temperatures during propagation suppress symptom expression, methods to detect low pathogen numbers in asymptomatic tissue are thus crucial (see Identification and detection).

Physical or chemical treatment of the planting material can decrease pathogen inoculum (Janse & Wenneker, 2002). Hot-water seed treatment reduced Xhortorum pvs carotae and gardneri infections. However, hot-water seed treatment can sometime be unsuitable. For example, a treatment at 50°C for 2 h of lettuce seeds against Xhortorum pv. vitians significantly reduced seed germination (Carisse et al., 2000). Some chemical seed treatments against this pathovar, such as soaking in 1% sodium hypochlorite for 5 min (Carisse et al., 2000), in 3% hydrogen peroxide for 5 min, or in suspensions of copper hydroxide plus mancozeb (Pernezny et al., 2002), were more effective in reducing seed contamination than others (copper hydroxide alone, benzoyl peroxide, or calcium peroxide). The seed treatments described above are limited to university or extension research and, to the best of our knowledge, are not found in official documents by the National Seed Health System (NSHS) or the International Seed Federation (ISF-ISHI). The use of seed treatments remains at the discretion of seed production companies, which must indicate what treatment was used on each seed lot.

Management of epiphytic Xhortorum (see Epidemiology) is challenging. Suppression methods of epiphytic Xhortorum pv. carotae on carrot foliage include sanitation and the use of drip irrigation to avoid wetting the phyllosphere during seed maturation (du Toit et al., 2005). Crop rotations or fallow periods could be used to eliminate contamination in plant debris by overwintering pathovars (Barak et al., 2001). In addition, good weed control and removing diseased plants can reduce inoculum amount (Barak et al., 2001; Toussaint et al., 2012), keeping in mind that some Xhortorum pathovars can survive epiphytically on weeds, and even infect them (see Epidemiology). Another good practice for decreasing the risk of disseminating Xhortorum pv. pelargonii involves not growing perennial Geranium spp. near greenhouse facilities producing Pelargonium spp. (Nameth et al., 1999).

Foliar applications of copper-based bactericides have been used for Xhortorum pvs carotae and vitians with variable efficacy depending on various factors (e.g., application time, disease development stage, and climate) (Bull & Koike, 2005; du Toit et al., 2005). Copper-based applications are unsustainable as they have adverse environmental effects, and because copper-induced resistant strains are problematic for sustainable, long-term control (Fishel, 2005; Husak, 2015; Willis & Bishop, 2016). For example, copper-induced resistance was reported in strains of Xhortorum pv. gardneri (Abbasi et al., 2015; Khanal et al., 2020). The use of nanoparticles was studied to manage copper-resistant and/or copper-tolerant strains. For example, silver (Ag) nanoparticles merged in a double-stranded DNA–graphene oxide matrix (Ag-dsDNA-GO) exhibited antibacterial activity against copper-tolerant Xhortorum pv. gardneri strains (Strayer, Oscoy, et al., 2016).

Biological control solutions against some Xhortorum pathovars have been proposed. For example, alternative nontoxic compounds that induce a systemic acquired resistance (SAR) in the host plant can provide a more environmentally sustainable approach to disease management than pesticides. The compound acibenzolar-S-methyl (ASM), a benzothiadiazole, released in Europe as Bion (Syngenta Ltd) and in the United States as Actigard 50WG (Syngenta Crop Protection Inc.), has shown positive results for controlling bacterial spot caused by Xhortorum pvs gardneri, pelargonii, and carotae (regarding the latter, the application was only successful on seeds) (Blainski et al., 2018; Pontes et al., 2016; Simmons et al., 2010; Yellareddygari et al., 2013). However, a limitation of ASM is its adverse effect on tomato growth and yield, which may be attributed to the energy cost associated with resistance induction (Romero et al., 2001).

Treating geranium leaves with methyl jasmonate inhibited multiplication of Xhortorum pv. pelargonii (Zhang, Grefer, et al., 2009) and spraying leaves with EPSs from Lactiplantibacillus plantarum triggered a local induced resistance in tomato leaves against Xhortorum pv. gardneri (Blainski et al., 2018). When tested on agar plates, various essential oils inhibited Xhortorum pathovars. Origanum compactum (oregano) and Thymus vulgaris (thyme) inhibited Xhortorum pv. pelargonii (Kokoskova & Pavela, 2006), and three oregano species (O. acutidens, O. rotundifolium, and O. vulgare) seemed to inhibit the growth of Xhortorum pvs pelargonii and vitians (Dadasoglu et al., 2011). Geraniin, a tannin extracted from sugar maple, resulted in high mortality of Xhortorum pv. vitians bacterial cells when tested by plate counting (Delisle-Houde et al., 2021).

Two P. syringae pv. syringae isolates, 422 and 17-049, decreased the colonization of Xhortorum pv. carotae on carrot leaves (Belvoir et al., 2019). Less virulent quorum-sensing mutants that elicit plant SAR might have a potential in management of Xhortorum pv. pelargonii (Barel et al., 2015). Bacteriophages applied as foliar sprays provided significant control of the disease caused by Xhortorum pv. gardneri in field trials (Balogh et al., 2003; Flaherty et al., 2000). However, bacteriophage effectiveness strongly depended on UV radiation and other environmental factors that affect their persistence in the phyllosphere (Iriarte et al., 2007). In greenhouse trials on potted geraniums, daily foliar sprays of bacteriophages significantly reduced disease caused by Xhortorum pv. pelargonii (Flaherty et al., 2001).


Resistance breeding research against Xhortorum has been focused on tomato, pepper, lettuce, carrot, and pelargonium, and multiple plant cultivars showed moderate to high resistance against the various pathovars. Wild tomatoes have a broad-spectrum resistance against multiple Xhortorum pv. gardneri strains (Liabeuf et al., 2015). Screening of S. lycopersicum and Solanum pimpinellifolium germplasm using HR identified partially resistant Slycopersicum lines, as well as three S. pimpinellifolium accessions (LA2533, LA1936, and PI 128,216) resistant against the pathovar. This resistance may be controlled by one to four loci with moderate heritability. The Spimpinellifolium lines were also resistant under field conditions (Liabeuf et al., 2015). Another wild tomato genotype, Slycopersicum var. cerasiforme line PI 114490, possessed broad-spectrum resistance to multiple xanthomonad pathogens, including Xhortorum pv. gardneri. Resistance in PI 114490 is quantitatively inherited, and QTL-3 locus and allele at QTL-11 are major contributors of resistance against Xhortorum pv. gardneri (Bernal et al., 2020).

A mutation in DMR6 (downy mildew resistance 6) in Arabidopsis, conferring broad-spectrum resistance to various Xanthomonas and Pseudomonas phythopathogens, was tested in tomato (Thomazella et al., 2016). The stable transgenic tomato plants were resistant against Xhortorum pv. gardneri and were not compromised in their growth and development.

In pepper, two dominant resistance genes, Bs3 and Bs7, are known to confer resistance against Xhortorum pv. gardneri strains carrying avirulence genes avrHah1 and avrBs7, respectively (Potnis et al., 2012; Schornack et al., 2008). However, the plasmidborne nature of both avirulence genes suggests vulnerability to resistance breakdown, so they have not been further considered in breeding programmes. Screening of core pepper germplasm collection against Xhortorum pv. gardneri revealed that more than 40 PI lines of Cbaccatum in greenhouse conditions and multiple PI lines of Cannuum showed promising resistance levels (Potnis et al., 2012). A total of 20 significant single nucleotide polymorphisms (SNPs), co-located within 150 kb of 92 unique genes, were recently identified against the pathovar (Potnis et al., 2019).

Regarding Xhortorum pv. vitians, different lettuce genotypes (Lsativa) show differential responses to the pathogen. For example, romaine and butterhead lettuce cultivars are among the highly susceptible ones (Pernezny et al., 1995). Moderately resistant cultivars include both green-leaf (e.g., Waldmann's Green and Grand Rapids) and red-leaf (e.g., Red Line) cultivars (Carisse et al., 2000), although other studies have noted their susceptibility (Bull et al., 2007). Such discrepancy could be due to differences in the experimental setups of the studies, such as using different strains for the pathogenicity tests. Other moderately resistant cultivars include Little Gem and Reine des Glaces (Batavia crisphead) (Bull et al., 2007). These two latter cultivars were deemed to be promising in breeding resistant cultivars against Xhortorum pv. vitians (Hayes, Trent, Mou, et al., 2014; Hayes, Trent, Truco, et al., 2014). However, undesirable traits (e.g., small size and low yield) associated with cv. Little Gem are of concern. Furthermore, this cultivar has also shown variable resistance in separate studies, making it an unattractive candidate (Bull et al., 2007; Lu & Raid, 2013). This difference could be due either to virulence dissimilarities at the strain level or to host susceptibility variation as a result of different environmental conditions at the cultivar evaluation locations (Lu & Raid, 2013). In addition, resistance of cv. Reine des Glaces was also highly dependent on environmental conditions (Bull et al., 2007).

Genetic maps of various wild lettuce species like Lserriola, L. saligna, and L. virosa, have revealed multiple genes conferring broad resistance (McHale et al., 2009; Truco et al., 2013). However, Lsaligna and Lvirosa have compatibility issues, making hybridization difficult. The broad resistance in wild lettuce species have yet to be tested against Xhortorum pv. vitians.

The high genetic variability of the pathogen population is a challenge for breeding cultivars with durable resistance. Resistance against MLSA-based groups B, D, and E of Xhortorum pv. vitians was identified to be controlled by a single dominant locus, Xanthomonas resistance 1 (Xar1), in the Batavia heirloom cv. La Brillante (Bull et al., 2016; Hayes, Trent, Mou, et al., 2014; Hayes, Trent, Truco, et al., 2014). Two other cultivars, Little Gem and Pavane, carry Xar1 alleles and are resistant to Californian isolates of Xhortorum pv. vitians. Another locus identified as Xcampestris vitians resistance (Xcvr) was found in the same linkage group (LG2) during the mapping of a PI 358001-1 × Tall Guzmaine population. The durability of Xar1 and Xcvr resistances in cv. La Brillante and PI 358001-1 raised concerns because of the high variability in the pathogen population (Hayes, Trent, Mou, et al., 2014; Hayes, Trent, Truco, et al., 2014). Major and minor quantitative trait loci (QTLs) controlling this resistance were identified and co-located in the same region of LG2 as previously identified with Xar1 and Xcvr (Sandoya et al., 2019).

A germplasm screening of carrot species (e.g., PI lines, public inbred lines, commercial cultivars, and wild varieties) indicated four PI lines (PI 263601, PI 418967, PI 432905, and PI 432906) and two of the wild relatives, Ames 7674 and SS10 OR, were the most resistant against Xhortorum pv. carotae (Christianson et al., 2015). The resistant PI lines are promising for use in commercial breeding programmes (Christianson et al., 2015).

In the genus Pelargonium, only a small number of pelargonium and geranium species have been screened for resistance against Xhortorum pv. pelargonii based on symptom expression alone after pathogen inoculation (Griesbach & Olbricht, 2002; Zhang, Sairam, et al., 2009). Five resistant pelargonium species were identified (Griesbach & Olbricht, 2002; Zhang, Sairam, et al., 2009), but most commercially important cultivars of Pelargonium zonale hybrids were highly susceptible (Griesbach & Olbricht, 2002; Zhang, Sairam, et al., 2009).


Several advances improving our understanding of the Xhortorum species have recently been published. However, some knowledge gaps remain, mainly related to extent of host range, detection, and control methods, including host resistance. Given the broad and diverse host range described for this species, it is likely that unreported hosts remain to be identified in various ecosystems. Further investigation of the natural and experimental host ranges of Xhortorum could provide insight into its evolutionary history and determine if plant domestication influenced host specialization of the pathovars of Xhortorum.

The recent increased availability of genomic data for Xhortorum will help in the identification of novel isolates from new natural hosts through establishing quick, field-deployable detection methods. Such tools will also be very beneficial for phytosanitary control, especially as prevention strategies are preferred to formulation applications and are less costly than containment and eradication measures.

There is a significant need to conduct a comprehensive comparative genomics analysis of this species, especially in view of the recent taxonomical changes. Because plasmids offer a potentially large source of variation in the species, determining the plasmid content of strains and their contribution to pathogenicity is highly relevant. The recent application of a TnSeq analysis in Xhortorum pv. vitians paves the way to functional genomics analysis of other Xhortorum members. Aside from providing insights into essential bacterial genes in different in vitro and in planta conditions, TnSeq would also considerably improve our understanding of Xhortorum biology.

Most important commercial varieties are still highly susceptible to diseases caused by Xhortorum. The inefficiency of application-based control strategies further consolidates host resistance as a promising area for devising practical and durable disease control solutions against Xhortorum. Because nonhost resistance is more durable than host resistance, screening more nonhost species for their disease response to Xhortorum could uncover broad, nonhost resistance genes against the pathovars. Furthermore, exploring recent advancements in the field of host resistance against bacteria, such as CRISPR/Cas9-mediated gene mutations, also sound promising for breeding Xhortorum-resistant plant cultivars. However, as highlighted throughout this pathogen profile, the high genetic variability of these phytopathogens affecting several plant families represents a real challenge for long-term resistance.


This article is based on work from COST Action CA16107 EuroXanth, supported by COST (European Cooperation in Science and Technology). N.C.D. was supported by grant no. IZCOZ0_177064 from the Swiss National Science Foundation (SNSF). L.M. was funded by a grant from the French Ministry of Higher Education, Research and Innovation. J.M.J. acknowledges the support by SCRI (grant no. 2020-51181-32154) from the USDA National Institute of Food and Agriculture and from Ohio Department of Agriculture Specialty Crops Block Grant (AGR-SCG-19-03). J.M.J. and E.B. are also grateful to support from USDA NIFA award no. 2018-67013-28490 through the NSF/NIFA Plant Biotic Interactions Program. N.P. acknowledges support by the SCRI (grant no. 2019-51181-30010) from the USDA National Institute of Food and Agriculture. J.F.P. acknowledges support from the Department of Life Sciences and Facility Management of the Zurich University of Applied Sciences (ZHAW) in Wädenswil. The authors thank John Bennett (ZHAW) for critically proofreading the manuscript.


    The authors declare that they have no competing interests.


    Data sharing is not applicable to this article as no new data were created or analysed in this study.