EPPO Global Database

'Candidatus Phytoplasma fraxini'(PHYPFR)

EPPO Datasheet: 'Candidatus Phytoplasma fraxini'

IDENTITY

Preferred name: 'Candidatus Phytoplasma fraxini'
Authority: Griffiths, Sinclair, Smart & Davis
Taxonomic position: Bacteria: Tenericutes: Mollicutes: Acholeplasmatales: Acholeplasmataceae
Other scientific names: Phytoplasma fraxini Griffiths, Sinclair, Smart & Davis
Common names in English: Ash yellows phytoplasma, AshY, Lilac witches' broom phytoplasma, lWB, witches' broom of lilac, yellows of ash
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Notes on taxonomy and nomenclature

Candidatus Phytoplasma fraxini’ formerly 16SrVII group or Ash Y, is a species that contains several strains: 16SrVII-A has been reported in North America, and 16SrVII-B, 16SrVII-C, 16SrVII-D, 16SrVII-E, 16SrVII-F, and 16SrVII-G in South America. However, the strain found in the central area of Colombia 16SrVII-G, which is believed to have originated in North America, is more similar to 16SrVII-A than to the strains described in South America (Griffiths et al., 1999; Barros et al., 2002; Flôres et al., 2015; Gajardo et al., 2009; da Silva et al., 2017; Franco-Lara et al., 2020).

EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: PHYPFR

HOSTS 2023-07-06

Candidatus Phytoplasma fraxini’ was initially reported in wild plants of the Oleaceae family affected with Ash yellows disease (AshY) and Lilac witches’-broom (LWB), in Canada and the United States. Susceptible species within the Fraxinus genus include F. americana (white ash), F. angustifolia, F. bungeana, F. excelsior (European ash), F. latifolia, F. nigra (black ash), F. ornus (flowering ash), F. pennsylvanica (green ash or red ash), F. potamophila, F. profunda, F. quadrangulata (blue ash), and F. velutina (Sinclair and Griffiths, 1994). Within the genus Syringa, plants of S. x diversifolia, S. x henryi, S. x josiflexa, S. josikaea, S. julianae, S. komarowii, S. laciniata, S. meyeri, S. microphylla, S. nanceiana, S. oblata, S. patula, S. persica, S. x prestoniae, S. sweginzowii, S. tomentella, S. villosa, S. vulgaris and S. yunnanensis have been reported as hosts (Sinclair and Griffiths, 1994; Sinclair et al., 1996, Walla et al., 2000).

In 2001, ‘Ca. P. fraxini’ was first reported in South America, infecting diseased urban Fraxinus uhdei (urapan) trees in Bogotá, Colombia (Griffiths et al., 2001). Evidence suggests it has moved from F. uhdei to other urban tree species such as Acacia melanoxylon (Fabaceae), Croton spp. (Euphorbiaceae), Eugenia neomyrtifolia (Myrtaceae), Liquidambar styraciflua (Altingiaceae), Magnolia grandiflora (Magnoliaceae), Pittosporum undulatum (Pittosporaceae), Populus nigra (Salicaceae), Sambucus nigra (Viburnaceae) and Salix humboldtiana (Salicaceae)) and Quercus humboldtii (Fagaceae) (Franco-Lara and Perilla-Henao, 2014; Franco-Lara et al., 2017, Franco-Lara, 2019). It also infects plants from several families in Cundinamarca, the Colombian department in which Bogotá is located. Susceptible plants include potato Solanum tuberosum (Solanaceae) and strawberry Fragaria x ananassa (Rosaceae) crops, and the grass Cenchrus clandestinus (Poaceae) and weeds Amaranthus dubius (Amaranthaceae), Cymbalaria muralis (Plantaginaceae), Fumaria capreolata (Papaveraceae), Holcus lanatus (Poaceae), Gnaphalium spicatum (Asteraceae), Gnaphalium cheiranthifolium (Asteraceae), Lepidium bipinnatifidum (Brassicaceae), Senecio vulgaris (Asteraceae), Sonchus oleraceus (Asteraceae) and Taraxacum officinale (Asteraceae) (Franco-Lara, 2019; Varela-Correa and Franco-Lara, 2020; Franco-Lara et al., 2023).

In Brazil, ‘Ca. P. fraxini’ has been found in natural infections in the Asteraceae Erigeron sp. and Vernonia brasiliana, and in the Apocynaceae Catharanthus roseus (Barros et al., 2002; Montano et al., 2014; Flôres et al., 2015; da Silva et al., 2017). In Argentina this bacterium is found associated with Argentinian alfalfa witches´-broom in Medicago sativa (Fabaceae) (Conci et al., 2005), strawberry (Fernández et al., 2013) and Asteraceae weeds Artemisia annua and Conyza bonariensis (Meneguzzi et al., 2008). In Chile, ‘Ca. P. fraxini’ has been detected in vineyards infecting Vitis vinifera (Vitaceae), and weeds such as Convolvulus arvensis (Convolvulaceae), Galega officinalis (Fabaceae), Gaultheria phillyreifolia (Ericaceae), Paeonia lactiflora (Paeoniaceae), Polygonum aviculare (Polygonaceae) and Ugni molinae (Myrtaceae) (Fiore et al., 2007; Arismendi et al., 2010; Arismendi et al., 2011: Gajardo et al., 2009; Longone et al., 2011).

Outside the Americas, ‘Ca. P. fraxini’ has been occasionally detected in Italy infecting grapevine (Zambon et al., 2018) and Hypericum perforatum (Hypericaceae) (Bruni et al., 2005), and in Iran in Phoenix dactylifera (Arecaceae) (Ghayeb Zamharir and Eslahi, 2019).

Experimental hosts include C. roseus, Cuscuta spp. (Convolvulaceae) (dodder), Daucus carota (Apiaceae), Phaseolus vulgaris (Fabaceae), and Trifolium pratense (Fabaceae) (Sinclair and Griffiths, 1996; Perilla-Henao et al., 2016).

Host list: Acacia melanoxylon, Amaranthus dubius, Artemisia annua, Cenchrus clandestinus, Convolvulus arvensis, Croton sp., Cymbalaria muralis, Erigeron bonariensis, Eugenia neomyrtifolia, Fragaria x ananassa, Fraxinus americana, Fraxinus angustifolia, Fraxinus bungeana, Fraxinus excelsior, Fraxinus latifolia, Fraxinus nigra, Fraxinus ornus, Fraxinus pennsylvanica, Fraxinus profunda, Fraxinus quadrangulata, Fraxinus sogdiana, Fraxinus uhdei, Fraxinus velutina, Fraxinus, Fumaria capreolata, Galega officinalis, Gamochaeta purpurea, Gaultheria phillyreifolia, Gnaphalium cheiranthifolium, Holcus lanatus, Hypericum perforatum, Lepidium bipinnatifidum, Liquidambar styraciflua, Magnolia grandiflora, Medicago sativa, Paeonia lactiflora, Phoenix dactylifera, Pittosporum undulatum, Polygonum aviculare, Populus nigra, Prunus sp., Pyrus sp., Quercus humboldtii, Salix humboldtiana, Sambucus nigra, Senecio vulgaris, Solanum tuberosum, Sonchus oleraceus, Syringa josikaea, Syringa julianae, Syringa komarowii, Syringa laciniata, Syringa meyeri, Syringa nanceiana, Syringa oblata, Syringa persica, Syringa pubescens subsp. microphylla, Syringa pubescens subsp. patula, Syringa tomentella subsp. sweginzowii, Syringa tomentella subsp. yunnanensis, Syringa tomentella, Syringa villosa, Syringa vulgaris, Syringa x diversifolia, Syringa x henryi, Syringa x josiflexa, Syringa x prestoniae, Syringa, Taraxacum officinale, Ugni molinae, Vernonanthura brasiliana, Vitis vinifera

GEOGRAPHICAL DISTRIBUTION 2023-07-06

EPPO Region: Italy (mainland)
Asia: Iran
North America: Canada (Alberta, Manitoba, Ontario, Québec, Saskatchewan), United States of America (Arizona, Colorado, Connecticut, Illinois, Indiana, Iowa, Kansas, Kentucky, Massachusetts, Michigan, Minnesota, Missouri, Montana, Nebraska, New Hampshire, New Jersey, New York, North Carolina, North Dakota, Ohio, Pennsylvania, South Dakota, Utah, Vermont, Virginia, West Virginia, Wisconsin, Wyoming)
South America: Argentina, Brazil (Minas Gerais, Parana, Rio de Janeiro, Sao Paulo), Chile, Colombia

BIOLOGY 2023-07-06

The epidemiology of ‘Ca. P. fraxini’ associated diseases has been described in detail for Bogotá and surrounding areas of Cundinamarca, in Colombia. In this area, ‘Ca. P. fraxini’ is usually present in mixed infections with ‘Candidatus Phytoplasma asteris’ related strains (Franco-Lara and Perilla-Henao, 2014; Perilla-Henao et al., 2016; Franco-Lara, 2019; Franco-Lara et al., 2020; Franco-Lara et al., 2023). At least two insect vectors are present in this area, Amplicephalus funzaensis and Exitianus atratus (both Hemiptera: Cicadellidae) (Perilla-Henao et al., 2016). These are polyphagous insect species that transmit both phytoplasmas and reproduce in the widespread grass species C. clandestinus. Other Cicadellidae species within the Deltocephalinae and Typhlocybinae are known to become infected with phytoplasmas but their ability to transmit these has not been tested (Perilla-Henao et al., 2016; Lamilla et al., 2022). C. clandestinus is an asymptomatic host of both ‘Ca. P. fraxini’ and ‘Ca. P. asteris´ and hosts not only A. funzaensis and E. atratus, but also other potential insect vectors.

Potential insect vectors in Canada include Graminella nigrifrons (Hemiptera: Cicadellidae) (Arocha-Rosete et al., 2011) and Paraphlepsius irroratus (Hemiptera: Cicadellidae) and spittlebug Philaenus spumarius (Hemiptera: Cercopidae) (Matteoni and Sinclair, 1988). In the United States, Scaphoideus spp. and Colladonus clitellarius (Hemiptera: Cicadellidae) (Hill and Sinclair, 2000) have both been detected as infected with phytoplasmas. In Chile, Paratanus exitiosus (Hemiptera: Cicadellidae) (Longone et al., 2011) is a potential insect vector of ‘Ca. P. fraxini’.

DETECTION AND IDENTIFICATION 2023-07-06

Symptoms

Symptoms vary between species, but some general features are observed. In susceptible taxa, Ash yellows and Lilac witches’-brooms are characterized by slow growth, loss of vitality, dieback (dead branches) and sometimes, early death of the plant. Other symptoms on trees species include light green or chlorotic foliage, witches´-brooms (proliferation of axilar shoots from one point that results in broom-like appearance), tufted foliage (branches with slow twig growth and short internodes that cause foliage to appear bunched), epicormic shoots (abnormal and disorderly proliferation of shoots that emerge from the trunk or branches), small leaves (leaves that never reach the normal leaf size), deliquescent branching (loss of apical dominance), abnormally elongated or shortened branches) which produce a deformation of the normal architecture of the tree crowns (Sinclair and Griffiths, 1994; Sinclair et al., 1996; Franco-Lara and Perilla-Henao, 2014; Lamilla et al., 2022).

In herbaceous plants such as potato, symptoms include leaf yellowing and curling, leaves with purple margins, excessive shoot proliferation and abnormally short or long internodes and leaves with altered shape and development (Varela-Correa and Franco-Lara, 2020; Franco-Lara et al., 2023). Infected strawberry plants show symptoms such as virescence, achenes’ hypertrophy and phyllody development that prevent the normal fruit formation (Perilla-Henao and Franco-Lara, 2012; Fernandez et al., 2013). In infected grapevines, symptoms vary with the plant variety; however, yellowing, downward rolling of leaves and leaf vein reddening are commonly observed (Gajardo et al., 2009). Alfalfa plants infected with Ca. P. fraxini’ can become stunted and develop small leaves, excessive shoot proliferation and flower abnormalities, although some plants are almost asymptomatic (Conci et al., 2005). In plants of infected Erigeron sp., Conyza bonariensis, Gaultheria phillyreifolia and Ugni molinae, the main symptom is the formation of witches´-brooms, while in Paeonia lactiflora, plant malformation, necrosis, leaf rolling and flower virescence and flower bud drying are observed (Barros et al., 2002; Meneguzzi et al., 2008; Arismendi et al., 2011). Some infected plants, such as the kikuyu grass C. clandestinus are completely asymptomatic (Franco-Lara, 2019).

Morphology

Electronic microscopy observations have shown the presence of pleomorphic translucid bodies of about 1 μM in the sieve tube elements or companion cells of infected potato plants and Andean oak (Q. humboldtii) trees infected with ‘Ca. P. fraxini’. These bodies were not observed in tissues other than the phloem. Using electronic microscopy, they were indistinguishable from other phytoplasmas (Lamilla et al., 2021; Franco Lara et al., 2023).

Detection and inspection methods

Symptoms are important evidence of the occurrence of phytoplasmas; however, their presence should be confirmed by molecular methods. The most common method of detection is amplification of the 16Sr RNA gene by PCR techniques. A commonly used method is detection of the 16SrRNA gene by nested PCR using universal primers for phytoplasmas (Bertaccini et al., 2019; Lee et al., 1993; Gundersen & Lee; 2006), followed by RFLP analysis or sequencing of the amplicon (Lee et al., 1998; Zhao et al., 2009). Real-time PCR methods have also been developed to detect ‘Ca. P. fraxini’ with universal primers (Christensen et al., 2004; Satta et al., 2017).

PATHWAYS FOR MOVEMENT 2023-07-06

Ca. P. fraxini’ is transmitted locally by insect vectors. Long distance spread of the pathogen can be caused by movement of infected material such as stem cuttings or seed-tubers. Grafting of infected material is also a possible pathway for phytoplasmas movement. There is no evidence of ‘Ca. P. dispersal by seeds.

PEST SIGNIFICANCE 2023-07-06

Economic impact

Several of the ‘Ca. P. fraxini’ susceptible species are tree or bushes of ornamental and ecological value in wild and urban forests. In these cases, the economic impact of the disease is mainly due to the negative impact on ecosystem services and loss of trees. Direct economic impact can occur in timber trees as well as in crops such as potato, strawberry, alfalfa, and grapevine, although the economic losses have not been estimated.

Control

Currently there are no curative methods against phytoplasma diseases, and resistance or tolerance to these pathogens is rare. Classical approaches include roguing, and insecticide treatments can be used against vectors, although these measures do not eliminate completely the source of inoculum. Integrated pest management strategies can be designed but require knowledge of the particularities of each pathosystem such as the susceptibility of the plant hosts, the insect vectors involved and their feeding habits. In economically important systems, symptoms and insect vector appearance should be permanently monitored to take further management decisions. For instance, tubers obtained from potato fields infected with phytoplasmas should not be used as seed-tubers for future planting seasons. Infected plants should not be used as propagating or grafting materials. Elimination of infected weeds is recommended, but it is not a definitive control measure. Using phytoplasma-free planting material should be a priority and molecular tests to confirm the absence of phytoplasmas in them is recommended.

Phytosanitary risk

´Ca. P. fraxini’ can infect plants in many botanical families. As with other phytoplasmas, its host range is more dependent on the feeding habits of the insect vectors than on the susceptibility of the plant hosts. The phytosanitary risk of ´Ca. P. fraxini’ relates to its ability to infect woody and herbaceous plants, but so far it has not been associated with any devastating disease.

PHYTOSANITARY MEASURES 2023-07-06

In the case of trees and crops, phytoplasma-free planting material should be used and, where appropriate should have been produced in the framework of a certification scheme. It may also be recommended that plants for planting originate from pest-free places of production.

REFERENCES 2023-07-06

Arismendi N, Andrade N, Riegel R & Carrillo R (2010) Presence of a phytoplasma associated with witches' broom disease in Ugni molinae Turcz. and Gaultheria phillyreifolia (Pers.) Sleumer determined by DAPI, PCR, and DNA sequencing. Chilean Journal of Agricultural Research 70, 26-33.

Arismendi N, Gonzalez F, Zamorano A, Andrade N, Pino AM & Fiore N (2011) Molecular identification of ‘Candidatus Phytoplasma fraxini’ in murta and peony in Chile. Bulletin of Insectology 64(Supplement), S95-S96.

Arocha-Rosete Y, Kent P, Agrawal V, Hunt D, Hamilton A, Bertaccini A, Scott J, Crosby W & Michelutti R (2011) Identification of Graminella nigrifrons as a potential vector for phytoplasmas affecting Prunus and Pyrus species in Canada. Canadian Journal of Plant Pathology 33, 465-474.

Bertaccini A, Paltrinieri S & Contaldo N (2019) Standard detection protocol: PCR and RFLP analyses based on 16S rRNA gene. In Phytoplasmas: Methods and Protocols, Methods in Molecular Biology (eds Musetti R & Pagliari L), volume 1875, pp. 83-95. Springer Science+Business Media, LLC, New York, USA.

Barros TS, Davis RE, Resende RO & Dally EL (2002) Erigeron witches'-broom phytoplasma in Brazil represents new subgroup VII-B in 16S rRNA gene group VII, the ash yellows phytoplasma group. Plant Disease 86, 1142-1148.

Bruni R, Pellati F, Bellardi MG, Benvenuti S, Paltrinieri S, Bertaccini A & Bianchi A (2005) Herbal drug quality and phytochemical composition of Hypericum perforatum L. affected by ash yellows phytoplasma infection. Journal of Agricultural and Food Chemistry 53, 964-968.

Christensen NM, Nicolaisen M, Hansen M & Schulz A (2004) Distribution of phytoplasmas in infected plants as revealed by real-time PCR and bioimaging. Molecular Plant-Microbe Interactions 17, 1175-1184.

Conci L, Meneguzzi N, Galdeano E, Torres L, Nome C & Nome S (2005) Detection and molecular characterisation of an alfalfa phytoplasma in Argentina that represents a new subgroup in the 16S rDNA ash yellows group (‘Candidatus Phytoplasma fraxini’). European Journal of Plant Pathology 113, 255-265.

da Silva Fugita J M, Pereira TBC, Banzato TC, Kitajima EW, da Souto ER & Bedendo IP (2017) Molecular characterization of a phytoplasma affiliated with the 16SrVII group representative of the novel 16SrVII-F subgroup. International Journal of Systematic and Evolutionary Microbiology 67, 3122-3126.

Fernández F D, Conci VC, Kirschbaum DS & Conci LR (2013) Molecular characterization of a phytoplasma of the ash yellows group occurring in strawberry (Fragaria x ananassa Duch.) plants in Argentina. European Journal of Plant Pathology 135, 1-4.

Fiore N, Prodan S, Paltrinieri S, Gajardo A, Botti S, Pino A M, Montealegre J & Bertaccini A (2007) Molecular characterization of phytoplasmas in Chilean grapevines. Bulletin of Insectology 60, 331.

Flôres D, Amaral Mello APDO, Pereira TBC, Rezende JAM & Bedendo IP (2015) A novel subgroup 16SrVII-D phytoplasma identified in association with erigeron witches' broom. International Journal of Systematic and Evolutionary Microbiology 65, 2761-2765.

Franco-Lara L (2019) Epidemiological aspects of phytoplasma diseases in a tropical country. Phytopathogenic Mollicutes 9, 45-46.

Franco-Lara L, Contaldo N, Mejia JF, Paltrinieri S, Duduk B & Bertaccini (2017) Detection and identification of phytoplasmas associated with declining Liquidambar styraciflua trees in Colombia. Tropical Plant Pathology 42, 352-361.

Franco-Lara L, García JA, Bernal YE & Rodríguez RA (2020) Diversity of the ‘Candidatus Phytoplasma asteris’ and ‘Candidatus Phytoplasma fraxini ’isolates that infect urban trees in Bogotá, Colombia. International Journal of Systematic and Evolutionary Microbiology 70, 6508-6517.

Franco-Lara L, Varela-Correa CA, Guerrero-Carranza GP & Quintero-Vargas JC (2023) Association of phytoplasmas with a new disease of potato crops in Cundinamarca, Colombia. Crop Protection 163, 106-123.

Franco-Lara L & Perilla-Henao LM (2014) Phytoplasma diseases in trees of Bogotá, Colombia: a serious risk for urban trees and Crops. In: Bertaccini A (ed) Phytoplasmas and Phytoplasma Disease Management: How to Reduce Their Economic Impact, 1 ed. Bologna: IPWG – COST, pp. 90–100.

Gajardo A, Fiore, N, Prodan S, Paltrinieri S, Botti S, Pino AM, Zamorano A, Montealegre J & Bertaccini A (2009) Phytoplasmas associated with grapevine yellows disease in Chile. Plant Disease 93, 789-796.

Ghayeb Zamharir M & Eslahi MR (2019) Molecular study of two distinct phytoplasma species associated with streak yellows of date palm in Iran. Journal of Phytopathology 167, 19-25.

Griffiths HM, Boa ER & Filgueira JJ (2001) Ash yellows disease of Fraxinus chinensis in Colombia. Phytopathology 91, S32-S33.

Griffiths HM, Sinclair WA, Smart CD & Davis RE (1999) The phytoplasma associated with ash yellows and lilac witches'-broom: ‘Candidatus Phytoplasma fraxini’. International Journal of Systematic and Evolutionary Microbiology 49, 1605-1614.

Gundersen DE & Lee IM (1996) Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathologia Mediterranea 35, 144-151.

Hill GT & Sinclair WA (2000) Taxa of leafhoppers carrying phytoplasmas at sites of ash yellows occurrence in New York State. Plant Disease 84, 134-138.

Lamilla J, Solano CJ & Franco‐Lara L (2022) Epidemiological characterization of a disease associated with phytoplasmas in Andean oak, Quercus humboldtii Bonpland, in Bogotá—Colombia. Forest Pathology 52, e12730.

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Varela-Correa CA & Franco-Lara L (2020) First report of a ‘Candidatus Phytoplasma fraxini’-related strain associated with potato in Colombia. Plant Disease 104, 2720-2720.

Walla JA, Jacobi WR, Tisserat NA, Harrell MO, Ball JJ, Neill GB, Reynard DA, Guo YH & Spiegel L (2000) Condition of green ash, incidence of ash yellows phytoplasmas, and their association in the Great Plains and Rocky Mountain regions of North America. Plant Disease 84, 268-274.

Zambon Y, Canel A, Bertaccini A & Contaldo N (2018) Molecular diversity of phytoplasmas associated with grapevine yellows disease in north-eastern Italy. Phytopathology 108, 206-214.

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Zunnoon‐Khan S, Arocha‐Rosete Y, Scott J, Crosby W, Bertaccini A & Michelutti R (2010) First report of ‘Candidatus Phytoplasma fraxini’ (group 16SrVII phytoplasma) associated with a peach disease in Canada. Plant Pathology 59, 1162.

ACKNOWLEDGEMENTS 2023-07-06

This datasheet was prepared in 2023 by Liliana Franco-Lara [Universidad Militar Nueva Granada, Bogotá, Colombia]. Her valuable contribution is gratefully acknowledged.

How to cite this datasheet?

EPPO (2024) 'Candidatus Phytoplasma fraxini'. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-21)

Datasheet history 2023-07-06

This datasheet was first published online in 2023. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.