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Candidatus Phytoplasma trifolii
(clover proliferation phytoplasma)

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Datasheet

Candidatus Phytoplasma trifolii (clover proliferation phytoplasma)

Summary

  • Last modified
  • 05 June 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Candidatus Phytoplasma trifolii
  • Preferred Common Name
  • clover proliferation phytoplasma
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Firmicutes
  •     Class: Mollicutes
  •       Order: Acholeplasmatales
  •         Family: Acholeplasmataceae
  • Summary of Invasiveness
  • The reference strain of ‘Ca. Phytoplasma trifolii’ is the causative agent of clover proliferation (CP) disease of alsike clover (Trifolium hybridum). The CP disease was first reported in Canada in the...

  • Principal Source
  • Draft datasheet under review

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Pictures

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PictureTitleCaptionCopyright
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induded purple top symptom in tomato.
TitleSymptoms
CaptionCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induded purple top symptom in tomato.
CopyrightPublic Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induded purple top symptom in tomato.
SymptomsCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induded purple top symptom in tomato.Public Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced big bud symptom in tomato.
TitleSymptoms
CaptionCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced big bud symptom in tomato.
CopyrightPublic Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced big bud symptom in tomato.
SymptomsCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced big bud symptom in tomato.Public Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced cauliflower like inflorescence in tomato.
TitleSymptoms
CaptionCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced cauliflower like inflorescence in tomato.
CopyrightPublic Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced cauliflower like inflorescence in tomato.
SymptomsCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced cauliflower like inflorescence in tomato.Public Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced witches broom growth in tomato.
TitleSymptoms
CaptionCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced witches broom growth in tomato.
CopyrightPublic Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)
Candidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced witches broom growth in tomato.
SymptomsCandidatus Phytoplasma trifolii (clover proliferation phytoplasma); symptoms, showing Ca. Phytoplasma trifolii BLTVA-induced witches broom growth in tomato.Public Domain - Released by the United States Department of Agriculture Agricultural Research Service (ARS)

Identity

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Preferred Scientific Name

  • Candidatus Phytoplasma trifolii Hiruki and Wang

Preferred Common Name

  • clover proliferation phytoplasma

Other Scientific Names

  • Phytoplasma trifolii

International Common Names

  • English: alfalfa witches'-broom phytoplasma; beet leafhopper-transmitted agent (BLTVA); potato purple top phytoplasma; potato witches'-broom phytoplasma; tomato big bud phytoplasma

EPPO code

  • PHYPTR

Summary of Invasiveness

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The reference strain of ‘Ca. Phytoplasma trifolii’ is the causative agent of clover proliferation (CP) disease of alsike clover (Trifolium hybridum). The CP disease was first reported in Canada in the early 1960s when the aetiological agent was mistakenly presumed to be a yellows-type virus (Chiykowski, 1965). Subsequent investigations revealed that the disease was associated with infection by a mycoplasma-like organism (Chen and Hiruki, 1975; Hiruki and Chen, 1984), now termed phytoplasma, strain CPR (Hiruki and Wang, 2004). Later, phytoplasmas of the same lineage (subgroup 16SrVI-A) were found in the USA, Mexico, and many countries in Europe and Asia, causing diseases in diverse leguminous and vegetable crops, responsible for significant yield losses and quality reductions. Phytoplasmas of the same lineage also caused disease in elm trees in the USA. Phytoplasmas of closely-related lineages (various subgroups of group 16SrVI) also have wide distributions around the world.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Firmicutes
  •         Class: Mollicutes
  •             Order: Acholeplasmatales
  •                 Family: Acholeplasmataceae
  •                     Genus: Phytoplasma
  •                         Species: Candidatus Phytoplasma trifolii

Notes on Taxonomy and Nomenclature

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Phytoplasmas are cell wall-less bacteria that infect vascular plants. Morphologically, phytoplasmas resemble animal- and human-infecting mycoplasmas therefore once had a trivial name, mycoplasma-like organism. On the basis of phylogenetic analysis of near full-length 16S rRNA gene sequences, phytoplasmas constitute a monophyletic clade within the Mollicutes (Gundersen et al., 1994) and are most closely related to members of the genus Acholeplasma within the Anaeroplasma clade (Weisburg et al., 1989). Despite decades of numerous attempts and recent progress (Contaldo et al., 2019), sustained axenic culture has not been demonstrated for any phytoplasma thus far. According to the convention for recording properties of uncultured organisms (Murray and Schleifer, 1994; Murray and Stackebrandt, 1995), a provisional genus ‘Candidatus Phytoplasma’ was erected to accommodate phytoplasmas (The International Research Programme for Comparative Mycoplasmology Phytoplasma/Spiroplasma Working Team - Phytoplasma Taxonomy Group, 2004). This provisional genus is embraced within the class Mollicutes, order Acholeplasmatales. ‘Candidatus Phytoplasma trifolii’ is one of the taxa established in the provisional genus and it was named after the plant host in which it was discovered, clover (Trifolium hybridum). Clover proliferation phytoplasma CPR is the reference (type) strain of the taxon (Hiruki and Wang, 2004).

In addition to Candidatus species assignment, phytoplasmas are also classified into groups and subgroups based on RFLP analysis of a 1.25 kb PCR-amplified 16S rDNA segment (F2nR2 fragment) using a defined set of 17 restriction enzymes (Lee et al., 1993; Lee et al., 1998). The phytoplasma groups delineated using this classification scheme are consistent with 16S rRNA gene phylogeny (Zhao et al., 2009). The 16S rDNA RFLP markers further separate phytoplasma strains in the same group into subgroup lineages. The phytoplasma 16S rDNA RFLP analysis also evolved from the original actual enzymatic approach to DNA sequence-based computational simulation (Wei et al., 2007; Zhao et al., 2009; Zhao and Davis, 2016). The reference strain of ‘Candidatus Phytoplasma trifolii’, CPR, is the initial member of the clover proliferation group, subgroup A (16SrVI-A) (Lee et al., 2000; Hiruki and Wang, 2004).

It was conceived that each phytoplasma 16Sr group should represent at least one species (Gundersen et al., 1994). Presently, ‘Ca. Phytoplasma trifolii’ is the only species recognized in the group 16SrVI. As each of the known members in the existing subgroups of 16SrVI shares >97.5% similarity with CPR in their 16S rDNA sequences, all current members in the group 16SrVI are considered ‘Ca. Phytoplasma trifolii’-related strains in this datasheet.

Description

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Like other phytoplasmas, ‘Ca. Phytoplasma trifolii’ resides in phloem sieve cells of infected plants and is transmitted from infected plants to healthy ones through phloem-feeding insects, mainly leafhoppers, planthoppers and psyllids. Phytoplasmas do not have a clearly defined shape (being amorphous); they may appear ovoid, oblong or filamentous under electron microscope. The size of phytoplasma cells ranges from 0.2 to 0.8 µm in diameter (Doi et al., 1967; McCoy et al., 1989; Weintraub and Beanland, 2006).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 05 Jun 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Asia

BangladeshPresentSiddique et al. (2001); EPPO (2020)Subgroup 16SrVI-D
ChinaPresentZhang Lei et al. (2020); Zhang Lei et al. (2012); EPPO (2020)Subgroup 16SrVI-A
-Inner MongoliaPresentZhang Lei et al. (2020); Zhang Lei et al. (2012); EPPO (2020)Subgroup 16SrVI-A
-YunnanPresentEPPO (2020)
IndiaPresent, WidespreadInvasiveManish Kumar et al. (2017); Ekta Khasa et al. (2016); EPPO (2020)Subgroups 16SrVI-D 16SrVI-H and undetermined 16SrVI subgroup lineages
-Andhra PradeshPresentInvasiveNaik et al. (2018); Ekta Khasa et al. (2016)Subgroup 16SrVI-D and an undetermined 16SrVI subgroup lineage
-AssamPresentInvasiveManish Kumar et al. (2017); Kalita et al. (2019)Subgroup 16SrVI-D
-BiharPresentInvasiveManish Kumar et al. (2017)Subgroup 16SrVI-D
-ChhattisgarhPresentInvasiveManish Kumar et al. (2017)Subgroup 16SrVI-D
-DelhiPresent, WidespreadInvasiveEkta Khasa et al. (2016); Ashutosh Rao et al. (2017); Manish Kumar et al. (2017); Gopala et al. (2018); Rihne et al. (2019)Subgroup 16SrVI-D
-GujaratPresentInvasiveKalaria et al. (2019)An undetermined 16SrVI subgroup lineage
-HaryanaPresentInvasiveEkta Khasa et al. (2016); Manish Kumar et al. (2017)Subgroup 16SrVI-D
-KarnatakaPresentInvasiveEkta Khasa et al. (2016); Venkataravanappa et al. (2018)Subgroup 16SrVI-D
-KeralaPresentInvasiveVandana Yadav et al. (2015)An undetermined 16SrVI subgroup lineage
-MaharashtraPresent, WidespreadInvasiveDas et al. (2016); Ekta Khasa et al. (2016); Manish Kumar et al. (2017)Subgroup 16SrVI-D
-OdishaPresent, WidespreadInvasiveSamad et al. (2006); Samad et al. (2008); Raj et al. (2009); Priya et al. (2010); Samad et al. (2011); Priya et al. (2016); Manish Kumar et al. (2017); Rao et al. (2018)Subgroups 16SrVI-D 16SrVI-H and undetermined 16SrVI subgroup lineages
-Uttar PradeshPresentInvasiveSingh et al. (2013); Gupta et al. (2010); Priya et al. (2010); Manish Kumar et al. (2017); Rao et al. (2018a)Subgroup 16SrVI-D and an undetermined 16SrVI subgroup lineage
IranPresent, WidespreadInvasiveBabaie et al. (2007); Hosseini et al. (2011); Fattahi et al. (2016); Hosseini et al. (2016); Zibadoost et al. (2016); Zamharir and Aldaghi (2018); Shahryari et al. (2019); EPPO (2020)Subgroups 16SrVI-A, 16SrVI-D, and undetermined 16SrVI subgroup lineages.
JapanAbsent, Unconfirmed presence record(s)EPPO (2020)
KazakhstanAbsent, Unconfirmed presence record(s)EPPO (2020)
LebanonPresentChoueiri et al. (2007); EPPO (2020)Subgroup 16SrVI-A
MalaysiaPresentTaylor et al. (2011)Subgroup 16SrVI-A
-SabahPresentTaylor et al. (2011)Subgroup 16SrVI-A
South KoreaPresentKim and Jung (2007); EPPO (2020)Subgroup 16SrVI-A
SyriaPresentEPPO (2020)
TurkeyPresentSertkaya et al. (2007); Özdemİr (2017); Usta et al. (2018); Serçe and Salih Yılmaz (2019); Yilmaz et al. (2019); EPPO (2020)Subgroup 16SrVI-A and undetermined 16SrVI subgroup lineages.
UzbekistanPresentEPPO (2020)

Europe

BulgariaAbsent, Unconfirmed presence record(s)EPPO (2020)
CzechiaAbsent, Unconfirmed presence record(s)EPPO (2020)
ItalyPresentFaggioli et al. (2004); Zambon et al. (2018); EPPO (2020)Subgroups 16SrVI-A and 16SrVI-D.
PolandAbsent, Invalid presence record(s)EPPO (2020)
RussiaPresentInvasiveGirsova et al. (2017); EPPO (2020)Subgroup 16SrVI-A
-Central RussiaPresentGirsova et al. (2017)Subgroup 16SrVI-A
-Russia (Europe)Absent, Unconfirmed presence record(s)EPPO (2020)
-Western SiberiaPresentInvasiveGirsova et al. (2017)Subgroup 16SrVI-A
SpainPresentCastro and Romero (2002); Alfaro-Fernández et al. (2017); EPPO (2020)Subgroup 16SrVI-A
United KingdomPresentWeintraub and Beanland (2006)16SrVI-A

North America

CanadaPresentInvasiveDeng et al. (1993); Khadhair and Hiruki (1995); Hiruki and Wang Keri (2004); EPPO (2020)Subgroups 16SrVI-A and 16SrVI-B.
-AlbertaPresentInvasiveHiruki and Wang Keri (2004); Deng and Hiruki (1991); Deng et al. (1993); Khadhair and Hiruki (1995); Khadhair et al. (1997); EPPO (2020)Subgroup 16SrVI-A.
-British ColumbiaAbsent, Unconfirmed presence record(s)EPPO (2020)
-New BrunswickAbsent, Unconfirmed presence record(s)EPPO (2020)
-Nova ScotiaAbsent, Unconfirmed presence record(s)EPPO (2020)
-OntarioAbsent, Unconfirmed presence record(s)EPPO (2020)
-Prince Edward IslandAbsent, Unconfirmed presence record(s)EPPO (2020)
-QuebecPresentJomantiene et al. (1998)Subgroup 16SrVI-B
-SaskatchewanAbsent, Unconfirmed presence record(s)EPPO (2020)
MexicoPresentReveles-Torres et al. (2018); Mauricio-Castillo et al. (2015); Salas-Muñoz et al. (2016); Swisher et al. (2017); Mauricio-Castillo et al. (2018); EPPO (2020)Subgroup 16SrVI-A
United StatesPresentInvasiveShaw et al. (1993); Jomantiene et al. (1998); Jacobs et al. (2003); Munyaneza et al. (2006); EPPO (2020)Subgroups 16SrVI-A, 16SrVI-B, 16SrVI-C, and an undetermined 16SrVI subgroup lineage.
-ArizonaAbsent, Unconfirmed presence record(s)EPPO (2020)
-CaliforniaPresentJomantiene et al. (1999); Shaw et al. (1993); EPPO (2020)Subgroup 16SrVI-A
-DelawarePresentFlower et al. (2018)Subgroup 16SrVI-A
-FloridaPresentJomantiene et al. (1998); EPPO (2020)Subgroup 16SrVI-B
-IdahoAbsent, Unconfirmed presence record(s)EPPO (2020)
-IllinoisPresentJacobs et al. (2003); EPPO (2020)Subgroup 16SrVI-C
-IowaAbsent, Unconfirmed presence record(s)EPPO (2020)
-MaineAbsent, Unconfirmed presence record(s)EPPO (2020)
-MarylandPresentJomantiene et al. (1999)Subgroup 16SrVI-A
-MichiganAbsent, Unconfirmed presence record(s)EPPO (2020)
-MinnesotaAbsent, Unconfirmed presence record(s)EPPO (2020)
-MontanaAbsent, Unconfirmed presence record(s)EPPO (2020)
-NevadaPresentFeng et al. (2019)An undetermined 16SrVI subgroup lineage
-New JerseyAbsent, Unconfirmed presence record(s)EPPO (2020)
-North DakotaPresentHiruki and Wang Keri (2004); EPPO (2020)Subgroup 16SrVI-A
-OhioPresentFlower et al. (2018); EPPO (2020)Subgroup 16SrVI-A
-OregonPresent, WidespreadInvasiveMurphy et al. (2014); Lee et al. (2004); Crosslin et al. (2005); Munyaneza et al. (2006); Munyaneza et al. (2007); Crosslin et al. (2012)Subgroup 16SrVI-A
-TexasAbsent, Unconfirmed presence record(s)EPPO (2020); Lee et al. (2001)
-UtahAbsent, Unconfirmed presence record(s)EPPO (2020)
-WashingtonPresent, WidespreadInvasiveMurphy et al. (2014); Lee et al. (2004); Lee et al. (2004a); Crosslin et al. (2005); Munyaneza et al. (2006); Munyaneza et al. (2007); Munyaneza et al. (2010); EPPO (2020)Subgroup 16SrVI-A
-West VirginiaAbsent, Unconfirmed presence record(s)EPPO (2020)
-WyomingAbsent, Unconfirmed presence record(s)EPPO (2020)

Oceania

AustraliaPresentWeintraub and Beanland (2006); EPPO (2020)16SrVI-A?
-New South WalesAbsent, Unconfirmed presence record(s)EPPO (2020)
-QueenslandAbsent, Unconfirmed presence record(s)EPPO (2020)
-South AustraliaAbsent, Unconfirmed presence record(s)EPPO (2020)
-TasmaniaAbsent, Unconfirmed presence record(s)EPPO (2020)
-VictoriaAbsent, Unconfirmed presence record(s)EPPO (2020)
-Western AustraliaAbsent, Unconfirmed presence record(s)EPPO (2020)

Risk of Introduction

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Ca. Phytoplasma trifolii’ and closely related phytoplasma strains in the clover proliferation group are not listed as quarantine pests by the European and Mediterranean Plant Protection Organization (EPPO).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedCultivated / agricultural land Present, no further details Harmful (pest or invasive)
Protected agriculture (e.g. glasshouse production) Present, no further details Harmful (pest or invasive)
Managed forests, plantations and orchards Present, no further details Harmful (pest or invasive)
Managed grasslands (grazing systems) Present, no further details Harmful (pest or invasive)
Rail / roadsides Present, no further details Harmful (pest or invasive)
Terrestrial ‑ Natural / Semi-naturalNatural forests Present, no further details Harmful (pest or invasive)
Natural grasslands Present, no further details Harmful (pest or invasive)
Riverbanks Present, no further details Harmful (pest or invasive)
Wetlands Present, no further details Harmful (pest or invasive)

Hosts/Species Affected

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Ca. Phytoplasma trifolii’ and closely related phytoplasma strains in the clover proliferation group have a broad range of hosts, affecting both dicotyledonous and monocotyledonous plants. Among commonly affected dicotyledonous hosts are agriculturally important leguminous, solanaceous and brassica crops such as lucerne, beans, clover, tomato, potato, pepper, brinjal, cabbage and mustard (Lee et al., 2004a; Lee et al., 2004b; Girsova et al., 2017; Kumari et al., 2019). Economically important monocotyledonous hosts include date palm and maize (Zibadoost et al., 2016; Zamharir and Eslahi, 2019). ‘Ca. Phytoplasma trifolii’ can also infect environmentally important ornamentals and forest trees; for the latter, an example is American elm, to which strains of ‘Ca. Phytoplasma trifolii’ can cause devastating elm yellows disease (Jacobs et al., 2003; Flower et al., 2018). It is worth noting that elm yellows disease can also be caused by another phytoplasma species, ‘Ca. Phytoplasma ulmi’.

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Allamanda cathartica (yellow allamanda)ApocynaceaeMain
Allium cepa (onion)LiliaceaeMain
Allium sativum (garlic)LiliaceaeOther
Amaranthus blitoides (spreading amaranth)AmaranthaceaeMain
Anemone (windflower)RanunculaceaeMain
Apium graveolens (celery)ApiaceaeMain
Araucaria heterophylla (norfolk Island pine)AraucariaceaeUnknown
Asclepias curassavica (bloodflower)AsclepiadaceaeMain
Azadirachta indica (neem tree)MeliaceaeMain
Beta vulgaris (beetroot)ChenopodiaceaeMain
Brassica juncea (mustard)BrassicaceaeMain
Brassica napusBrassicaceaeMain
Brassica napus var. oleiferaBrassicaceaeOther
Brassica oleracea (cabbages, cauliflowers)BrassicaceaeMain
Calotropis gigantea (Yercum fibre)ApocynaceaeOther
Calotropis gigantea (Yercum fibre)ApocynaceaeMain
Cannabis sativa subsp. sativaCannabaceaeMain
Capsella bursa-pastoris (shepherd's purse)BrassicaceaeMain
Capsicum annuum (bell pepper)SolanaceaeMain
Carthamus tinctorius (safflower)AsteraceaeMain
Catharanthus roseus (Madagascar periwinkle)ApocynaceaeMain
Celosia argentea (celosia)AmaranthaceaeMain
Centaurea solstitialis (yellow starthistle)AsteraceaeMain
Cicer arietinum (chickpea)FabaceaeMain
Citrus reticulata (mandarin)RutaceaeMain
Conyza canadensis (Canadian fleabane)AsteraceaeMain
CosmosAsteraceaeMain
Croton bonplandianusEuphorbiaceaeMain
Cucumis sativus (cucumber)CucurbitaceaeMain
Cucurbita (pumpkin)CucurbitaceaeMain
Datura innoxia (downy thorn apple)SolanaceaeMain
Datura stramonium (jimsonweed)SolanaceaeMain
Fragaria ananassa (strawberry)RosaceaeMain
Fragaria chiloensis (Chilean strawberry)RosaceaeMain
Fragaria virginiana (scarlet strawberry (UK))RosaceaeMain
Gladiolus grandiflorusIridaceaeMain
Glycine max (soyabean)FabaceaeOther
Glycine max (soyabean)FabaceaeMain
Guizotia abyssinica (niger)AsteraceaeMain
Helianthus annuus (sunflower)AsteraceaeMain
Hibiscus rosa-sinensis (China-rose)MalvaceaeMain
Juniperus procumbensCupressaceaeMain
Lactuca sativa (lettuce)AsteraceaeMain
Lavandula (lavender)LamiaceaeMain
Lens culinaris subsp. culinaris (lentil)FabaceaeMain
Lupinus polyphyllus (garden lupin)FabaceaeMain
Medicago sativa (lucerne)FabaceaeMain
Melilotus albus (honey clover)FabaceaeMain
Phaseolus vulgaris (common bean)FabaceaeMain
Phoenix dactylifera (date-palm)ArecaceaeMain
Physalis ixocarpaSolanaceaeMain
Portulaca grandiflora (Rose moss)PortulacaceaeMain
Portulaca oleracea (purslane)PortulacaceaeMain
Prunus amygdalusRosaceaeMain
Prunus avium (sweet cherry)RosaceaeMain
Prunus persica (peach)RosaceaeMain
Raphanus sativus (radish)BrassicaceaeMain
Rubia tinctorum (Rose madder)RubiaceaeMain
Salix alba (white willow)SalicaceaeMain
Salix babylonica (weeping willow)SalicaceaeMain
Salix bebbiana (Bebb willow)SalicaceaeMain
Salix discolorSalicaceaeMain
Salix exigua (sandbar willow)SalicaceaeMain
Salix petiolaris (Meadow willow)SalicaceaeMain
Salsola kali (common saltwort)ChenopodiaceaeMain
Saponaria officinalis (soapwort)CaryophyllaceaeMain
Sauropus androgynusEuphorbiaceaeOther
Sauropus androgynusEuphorbiaceaeMain
Senecio vulgarisAsteraceaeMain
Sesamum indicum (sesame)PedaliaceaeMain
Setaria verticillata (bristly foxtail)PoaceaeMain
Solanum lycopersicum (tomato)SolanaceaeMain
Solanum melongena (aubergine)SolanaceaeMain
Solanum tuberosum (potato)SolanaceaeMain
Sorghum halepense (Johnson grass)PoaceaeMain
Trachyspermum ammiApiaceaeMain
Trifolium (clovers)FabaceaeMain
Trifolium hybridum (alsike clover)FabaceaeMain
Typha angustifolia (lesser bulrush)TyphaceaeMain
Ulmus americana (American elm)UlmaceaeMain
Verbesina encelioides (golden crownbeard)AsteraceaeMain
Vicia faba (faba bean)FabaceaeMain
Vitis vinifera (grapevine)VitaceaeMain
Withania somnifera (poisonous gooseberry)SolanaceaeMain
Zea mays (maize)PoaceaeMain

Growth Stages

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Symptoms

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Infection by ‘Ca. Phytoplasma trifolii’ or other phytoplasma strains in the clover proliferation group induces a wide variety of symptoms in hosts. Symptom types differ depending on host species and stages of infection. Most frequently observed symptoms during vegetative growth stage include shoot proliferation, witches’-broom growth, little leaf, leaf yellowing and stunting. Prominent floral symptoms include virescence, phyllody, big bud and flower multiplication. Results from studies on potato purple top (PPT) phytoplasma (subgroup 16SrVI-A) infection in tomato revealed a profound disruption of gibberellin homeostasis in host plants (Ding et al., 2013a; Ding et al., 2013b). It was discovered that PPT phytoplasma infection can derail plant meristem cells from their genetically pre-programmed destiny, therefore altering the growth and developmental pattern of the host plant (Wei et al., 2013). Studies revealed that PPT phytoplasma was able to induce multiple symptoms in a single tomato plant sequentially - a total of eight mutually distinct symptoms (witches'-broom growth, disrupted sympodial growth pattern, cauliflower-like inflorescence, big bud, virescence, floral organ duplication, parthenocarpy and vivipary) were identified. Each symptom was linked to a stage-specific event of apical meristem destiny derailment and corresponding transcriptional reprogramming (Wei et al., 2013; Wei et al., 2019).

In addition to inducing visible symptoms (morphological changes), ‘Ca. Phytoplasma trifolii’ infection can also induce profound physiological changes in host plants. Studies revealed that a pepper-infecting strain (also a member of subgroup 16SrVI-A) was able to alter the metabolic activities of the host, resulting in a progressive increase in an array of secondary metabolites including phenolic compounds, flavonoids, condensed tannins and anthocyanins (Reveles-Torres et al., 2018b); the phytoplasma infection also reduced CO2 fixation, decreased invertase activity, inhibited glycolysis, and altered sugar and amino acid compositions in the host tissues (Velásquez-Valle et al., 2019).

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal patterns
Fruit / abnormal shape
Fruit / discoloration
Fruit / premature drop
Fruit / reduced size
Growing point / discoloration
Growing point / distortion
Inflorescence / abnormal leaves (phyllody)
Inflorescence / discoloration (non-graminaceous plants)
Inflorescence / distortion (non-graminaceous plants)
Inflorescence / twisting and distortion
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / leaves rolled or folded
Leaves / yellowed or dead
Roots / reduced root system
Stems / dieback
Stems / distortion
Stems / stunting or rosetting
Stems / witches broom
Whole plant / discoloration
Whole plant / dwarfing
Whole plant / early senescence
Whole plant / plant dead; dieback
Whole plant / wilt

Biology and Ecology

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Phytoplasmas are nutritionally fastidious. There is no indication that any phytoplasma can survive outside of its host; no pure phytoplasma culture has been established in any cell-free medium thus far. In nature, like other phytoplasmas, ‘Ca. Phytoplasma trifolii’ reference strain CPR and other related strains in the clover proliferation group (16SrVI) are transmitted by phloem-feeding insect vectors. It has been demonstrated that the reference strain CPR (type member of subgroup 16SrVI-A) is transmitted from clover (Trifolium hybridum) to other plants by Macrosteles fascifrons (Chiykowski, 1965; Hiruki and Wang, 2004). In the Pacific northwest of the USA, BLTVA phytoplasma (also belonging to subgroup 16SrVI-A) has a broad range of hosts including potato, tomato, radish, carrot, sugarbeet, dry bean, groundsel, kochia and shepherd’s purse. BLTVA phytoplasma is mainly transmitted by beef leafhopper Circulifer tenellus (Crosslin et al., 2005; Munyaneza et al., 2006; Munyaneza et al., 2007; Munyaneza et al., 2010; Crosslin et al., 2012; Murphy et al., 2014). Under experimental conditions, C. tenellus was able to transmit BLTVA phytoplasma among 43 plant species belonging to at least 14 different families (Golino et al., 1989). In Mexico, subgroup 16SrVI-A phytoplasmas are reportedly transmitted by leafhoppers Ceratagallia nitidula and Empoasca abrupta (Salas-Muñoz et al., 2018). In Russia, leafhoppers Euscelis incisa and Aphrodes bicinctus have been implicated in transmitting 16SrVI-A phytoplasmas among various leguminous crops (Girsova et al., 2017). In Iran, leafhoppers Circulifer haematoceps [Neoaliturus haematoceps] and Orosius albicinctus [Orosius orientalis] are potential vectors for transmitting subgroup 16SrVI-A phytoplasmas that affect various plants including sesame, cabbage and golden marguerite (Salehi et al., 2007; Salehi et al., 2017; Hemmati et al., 2018). In India, where phytoplasmas of the subgroup 16SrVI-D are prevalent, leafhopper Hishimonus phycitis has been identified as a potential vector (Kumar et al., 2017; Gopala et al., 2018). In addition, according to earlier studies (as reviewed by Weintraub and Beanland, 2006, and references therein), Orosius argentatus, Batracomorphus punctatus and Euscelis spp. were also involved in transmitting clover proliferation group (16SrVI) phytoplasmas.

Means of Movement and Dispersal

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Vector Transmission (Biotic)

In nature, ‘Ca. Phytoplasma trifolii’, including other closely related 16SrVI phytoplasma strains, is transmitted by phloem-feeding insect vectors. Macrosteles fascifrons and Circulifer tenellus are confirmed major vectors (Golino et al., 1989; Hiruki and Wang, 2004; Munyaneza et al., 2006). Other potential vectors include Aphrodes bicinctus, Batracomorphus punctatus, Ceratagallia nitidula, Circulifer haematoceps [Neoaliturus haematoceps], Empoasca abrupta, Euscelis incisa, Hishimonus phycitis, Orosius albicinctus [Orosius orientalis] and O. argentatus (Weintraub and Beanland, 2006; Salehi et al., 2007; Girsova et al., 2017; Kumar et al., 2017; Salehi et al., 2017; Gopala et al., 2018; Hemmati et al., 2018; Salas-Muñoz et al., 2018).

Natural Dispersal

Generally, abiotic factors are not involved in natural dispersal of phytoplasmas. However, it has been noted that atmospheric structure and motions could influence insect migration (Drake and Farrow, 1988). Low-level jet stream wind-facilitated long-range movement of phytoplasma-infected aster leafhopper (M. fascifrons) was reported (MacRae, 2014) although ‘Ca. Phytoplasma trifolii’ was not specifically mentioned.

Accidental Introduction

Ca. Phytoplasma trifolii’ is not seed transmittable but can be spread through propagules such as tubers, runners, bulbs and cuttings. The pathogen may be accidentally introduced into new areas by moving vegetatively propagated plant materials that are already infected but are asymptomatic.

Ca. Phytoplasma trifolii’ can also be transmitted through graft union from an infected component to a healthy component.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Breeding and propagation Yes Yes
Crop production Yes Yes
Cut flower trade Yes Yes
Nursery trade Yes Yes
Ornamental purposes Yes Yes
People sharing resources Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Germplasm Yes Yes
Host and vector organisms Yes Yes
Plants or parts of plants Yes Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Bark Yes Pest or symptoms usually invisible
Bulbs/Tubers/Corms/Rhizomes Yes Pest or symptoms usually invisible
Flowers/Inflorescences/Cones/Calyx Yes Pest or symptoms usually invisible
Leaves Yes Pest or symptoms usually invisible
Roots Yes Pest or symptoms usually invisible
Seedlings/Micropropagated plants Yes Pest or symptoms usually invisible
Stems (above ground)/Shoots/Trunks/Branches Yes Pest or symptoms usually invisible
Plant parts not known to carry the pest in trade/transport
Fruits (inc. pods)
Growing medium accompanying plants
True seeds (inc. grain)
Wood

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Aphrodes bicinctusGirsova et al., 2017. InsectRussian Federation
Batracomorphus punctatusWeintraub and Beanland, 2006. InsectAustralia
Ceratagallia nitidulaSalas-Muñoz et al., 2018. InsectMexico
Circulifer tenellus2007; 2012); Munyaneza et al., ; Golino et al., 1989; 2010); Murphy et al., 2014. InsectUSA
Empoasca abruptaSalas-Muñoz et al., 2018. InsectMexico
Euscelis incisaWeintraub and Beanland, 2006. InsectUK
Hishimonus phycitisGopala et al., 2018. InsectIndia
Macrosteles fascifronsHiruki and Wang, 2004. InsectUSA
Neoaliturus haematocepsSalehi et al., 2017. InsectIran
Neoaliturus pulcherSeyahooei et al., 2017. InsectIran
Orosius argentatusWeintraub and Beanland, 2006. InsectAustralia
Orosius orientalisSalehi et al., 2017. InsectTurkey

Impact Summary

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CategoryImpact
Economic/livelihood
Environment (generally)

Economic Impact

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Ca. Phytoplasma trifolii’ and other phytoplasma strains in the clover proliferation group (16SrVI) cause diseases in a variety of agriculturally important plant species including leguminous, solanaceous and brassica crops, inflicting commodity yield losses and quality reductions. Economic impacts vary year to year and location to location depending largely on population dynamics of the transmission vectors. Taking BLTVA phytoplasma-induced potato purple top disease in the Pacific northwest of the USA as an example, one study revealed that there was a mean decrease in potato tuber yield of “0-12% at a density of one beef leafhopper per plant, 6-19% at two beet leafhoppers per plant, and 6-20% for five beet leafhoppers per plant” (Murphy et al., 2014).

Diagnosis

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Presently, the most efficient and accurate way to detect and identify ‘Ca. Phytoplasma trifolii’ is PCR-amplification of phytoplasmal 16S rRNA gene fragment and subsequent DNA sequencing of the amplicon. The sensitivity of phytoplasma detection can be enhanced by using two-step enriched-nested PCR technique. The most commonly used phytoplasma-universal primer pairs for two-step nested PCR technique PCRs include P1A/16S-SR (Lee et al., 2004c) and R16F2n/R16R2 (Lee et al., 1993; Gundersen and Lee, 1996). After DNA sequencing of the amplicons, an iPhyClassifier analysis online (Zhao et al., 2009; https://plantpathology.ba.ars.usda.gov/cgi-bin/resource/iphyclassifier.cgi) can help to determine whether an infecting phytoplasma is affiliated with ‘Ca. Phytoplasma trifolii’.

Detection and Inspection

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Field visual survey is useful for a rapid assessment of overall health conditions of the plants in the field and the extent of possible phytoplasma infections (see Symptoms). However, as mutually distinct phytoplasma species may induce similar symptoms, it is necessary to conduct laboratory diagnostic tests on field samples to confirm phytoplasma infection and to identify ‘Ca. Phytoplasma trifolii’.

Similarities to Other Species/Conditions

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Mutually distinct phytoplasma species may induce the plant disease or diseases with indistinguishable symptoms. Several plant diseases that are caused by ‘Ca. Phytoplasma trifolii’ infection can also be caused by infection of some other Candidatus phytoplasma species. For example, the aetiological agent of elm yellows disease can either be ‘Ca. Phytoplasma trifolii’ (Jacobs et al., 2003; Flower et al., 2018) or ‘Ca. Phytoplasma ulmi’ (Griffiths et al., 1999; Lee et al., 2004c). Likewise, the causative agent of potato purple top disease can either be ‘Ca. Phytoplasma trifolii’ (BLTVA, Crosslin et al., 2005) or a number of other Candidatus phytoplasma species including ‘Ca. Phytoplasma asteris’ and ‘Ca. Phytoplasma aurantifolia’ (Kumari et al., 2019). In such cases, laboratory tests (PCR-amplification of phytoplasmal 16S rRNA gene and subsequent DNA sequencing of the amplicon) are necessary to identify the infecting phytoplasma. The signature sequences defined in the formal descriptions of ‘Ca. Phytoplasma trifolii’ (Hiruki and Wang, 2004) will be helpful in distinguishing ‘Ca. Phytoplasma trifolii’ from other phytoplasma species.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

There is no cure for phytoplasmal diseases. Good agricultural practices, such as the use of healthy plant materials, removal of diseased plants, eradication of potential phytoplasma reservoirs (weeds) and control of insect vectors, can help in preventing and managing diseases caused by ‘Ca. Phytoplasma trifolii’.

References

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14/05/20 Original text:

Yan Zhao, Molecular Plant Pathology Laboratory, Agricultural Research Service-USDA, Beltsville, MD 20705, USA.

Wei Wei, Molecular Plant Pathology Laboratory, Agricultural Research Service-USDA, Beltsville, MD 20705, USA.

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