Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Candidatus Phytoplasma trifolii
(clover proliferation phytoplasma)

Zhao Yan and Wei Wei, 2020. Candidatus Phytoplasma trifolii (clover proliferation phytoplasma). Invasive Species Compendium. Wallingford, UK: CABI. DOI:10.1079/ISC.40854.20210200691

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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 early 1960s when the aetiolo...

  • 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-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)
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)

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: 23 Jul 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Asia

BangladeshPresentSubgroup 16SrVI-D
ChinaPresentSubgroup 16SrVI-A
-Inner MongoliaPresentSubgroup 16SrVI-A
-YunnanPresent
IndiaPresent, WidespreadInvasiveSubgroups 16SrVI-D 16SrVI-H and undetermined 16SrVI subgroup lineages
-Andhra PradeshPresentInvasiveSubgroup 16SrVI-D and an undetermined 16SrVI subgroup lineage
-AssamPresentInvasiveSubgroup 16SrVI-D
-BiharPresentInvasiveSubgroup 16SrVI-D
-ChhattisgarhPresentInvasiveSubgroup 16SrVI-D
-DelhiPresent, WidespreadInvasiveSubgroup 16SrVI-D
-GujaratPresentInvasiveAn undetermined 16SrVI subgroup lineage
-HaryanaPresentInvasiveSubgroup 16SrVI-D
-KarnatakaPresentInvasiveSubgroup 16SrVI-D
-KeralaPresentInvasiveAn undetermined 16SrVI subgroup lineage
-MaharashtraPresent, WidespreadInvasiveSubgroup 16SrVI-D
-OdishaPresent, WidespreadInvasiveSubgroups 16SrVI-D 16SrVI-H and undetermined 16SrVI subgroup lineages
-Uttar PradeshPresentInvasiveSubgroup 16SrVI-D and an undetermined 16SrVI subgroup lineage
IranPresent, WidespreadInvasiveSubgroups 16SrVI-A, 16SrVI-D, and undetermined 16SrVI subgroup lineages.
JapanAbsent, Unconfirmed presence record(s)
KazakhstanAbsent, Unconfirmed presence record(s)
LebanonPresentSubgroup 16SrVI-A
MalaysiaPresentSubgroup 16SrVI-A
-SabahPresentSubgroup 16SrVI-A
OmanPresent
South KoreaPresentSubgroup 16SrVI-A
SyriaPresent
TurkeyPresentSubgroup 16SrVI-A and undetermined 16SrVI subgroup lineages.
UzbekistanPresent

Europe

BulgariaAbsent, Unconfirmed presence record(s)
CzechiaAbsent, Unconfirmed presence record(s)
ItalyPresentSubgroups 16SrVI-A and 16SrVI-D.
PolandAbsent, Invalid presence record(s)
RussiaPresentInvasiveSubgroup 16SrVI-A
-Central RussiaPresentSubgroup 16SrVI-A
-Russia (Europe)Absent, Unconfirmed presence record(s)
-Western SiberiaPresentInvasiveSubgroup 16SrVI-A
SpainPresentSubgroup 16SrVI-A
United KingdomPresent16SrVI-A

North America

CanadaPresentInvasiveSubgroups 16SrVI-A and 16SrVI-B.
-AlbertaPresentInvasiveSubgroup 16SrVI-A.
-British ColumbiaAbsent, Unconfirmed presence record(s)
-New BrunswickAbsent, Unconfirmed presence record(s)
-Nova ScotiaAbsent, Unconfirmed presence record(s)
-OntarioAbsent, Unconfirmed presence record(s)
-Prince Edward IslandAbsent, Unconfirmed presence record(s)
-QuebecPresentSubgroup 16SrVI-B
-SaskatchewanAbsent, Unconfirmed presence record(s)
MexicoPresentSubgroup 16SrVI-A
United StatesPresentInvasiveSubgroups 16SrVI-A, 16SrVI-B, 16SrVI-C, and an undetermined 16SrVI subgroup lineage.
-ArizonaAbsent, Unconfirmed presence record(s)
-CaliforniaPresentSubgroup 16SrVI-A
-FloridaPresentSubgroup 16SrVI-B
-IdahoAbsent, Unconfirmed presence record(s)
-IllinoisPresentSubgroup 16SrVI-C
-IowaAbsent, Unconfirmed presence record(s)
-MaineAbsent, Unconfirmed presence record(s)
-MarylandPresentSubgroup 16SrVI-A
-MichiganAbsent, Unconfirmed presence record(s)
-MinnesotaAbsent, Unconfirmed presence record(s)
-MontanaAbsent, Unconfirmed presence record(s)
-NevadaPresentAn undetermined 16SrVI subgroup lineage
-New JerseyAbsent, Unconfirmed presence record(s)
-North DakotaPresentSubgroup 16SrVI-A
-OhioPresentSubgroup 16SrVI-A
-OregonPresent, WidespreadInvasiveSubgroup 16SrVI-A
-TexasAbsent, Unconfirmed presence record(s)
-UtahAbsent, Unconfirmed presence record(s)
-WashingtonPresent, WidespreadInvasiveSubgroup 16SrVI-A
-West VirginiaAbsent, Unconfirmed presence record(s)
-WyomingAbsent, Unconfirmed presence record(s)

Oceania

AustraliaPresent16SrVI-A?
-New South WalesAbsent, Unconfirmed presence record(s)
-QueenslandAbsent, Unconfirmed presence record(s)
-South AustraliaAbsent, Unconfirmed presence record(s)
-TasmaniaAbsent, Unconfirmed presence record(s)
-VictoriaAbsent, Unconfirmed presence record(s)
-Western AustraliaAbsent, Unconfirmed presence record(s)

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 ManagedCultivated / agricultural land Present, no further details Harmful (pest or invasive)
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Present, no further details Harmful (pest or invasive)
Terrestrial ManagedManaged forests, plantations and orchards Present, no further details Harmful (pest or invasive)
Terrestrial ManagedManaged grasslands (grazing systems) Present, no further details Harmful (pest or invasive)
Terrestrial ManagedRail / roadsides Present, no further details Harmful (pest or invasive)
Terrestrial Natural / Semi-naturalNatural forests Present, no further details Harmful (pest or invasive)
Terrestrial Natural / Semi-naturalNatural grasslands Present, no further details Harmful (pest or invasive)
Terrestrial Natural / Semi-naturalRiverbanks Present, no further details Harmful (pest or invasive)
Terrestrial Natural / Semi-naturalWetlands 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 nameFamilyContextReferences
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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                                                                                                                                                                            Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

                                                                                                                                                                            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. (2006; Golino et al. (1989); Shaw et al. (1993); Crosslin et al. (2005; 2010); Murphy et al. (2014); Weintraub and Beanland (2006); Swisher et al. (2017)InsectMexico; USA
                                                                                                                                                                            Empoasca abruptaSalas-Muñoz et al. (2018)InsectMexico
                                                                                                                                                                            Euscelis incisaWeintraub and Beanland (2006); Girsova et al. (2017)InsectRussian Federation; UK
                                                                                                                                                                            Hishimonus phycitisGopala et al. (2018)InsectIndia
                                                                                                                                                                            Macrosteles fascifronsHiruki and Wang (2004)InsectCanada; USA
                                                                                                                                                                            Neoaliturus haematocepsSalehi et al. (2017)InsectIran
                                                                                                                                                                            Neoaliturus pulcherSeyahooei et al. (2017)InsectIran
                                                                                                                                                                            Orosius argentatusWeintraub and Beanland (2006)InsectAustralia
                                                                                                                                                                            Orosius orientalisSalehi et al. (2017); Hemmati et al. (2018); Sertkaya et al. (2007); Özdemir (2017)InsectIran; Turkey

                                                                                                                                                                            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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                                                                                                                                                                            Reveles-Torres, L. R., Velásquez-Valle, R., Salas-Muñoz, S., Mauricio-Castillo, J. A., Esqueda-Dávila, K. C. J., Herrera, M. D., 2018. Candidatus Phytoplasma trifolii (16SrVI) infection modifies the polyphenols concentration in pepper (Capsicum annuum) plant tissues. Journal of Phytopathology, 166(7/8), 555-564. https://onlinelibrary.wiley.com/journal/14390434

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                                                                                                                                                                            Salehi, M., Hosseini, S. A. E., Salehi, E., Bertaccini, A., 2017. Genetic diversity and vector transmission of phytoplasmas associated with sesame phyllody in Iran. Folia Microbiologica, 62(2), 99-109. doi: 10.1007/s12223-016-0476-5

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                                                                                                                                                                            Draft datasheet under review

                                                                                                                                                                            Contributors

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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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