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Candidatus Phytoplasma pini
(pine witches'-broom phytoplasma)

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Datasheet

Candidatus Phytoplasma pini (pine witches'-broom phytoplasma)

Summary

  • Last modified
  • 10 May 2019
  • Datasheet Type(s)
  • Documented Species
  • Pest
  • Preferred Scientific Name
  • Candidatus Phytoplasma pini
  • Preferred Common Name
  • pine witches'-broom phytoplasma
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Firmicutes
  •     Class: Mollicutes
  •       Order: Acholeplasmatales
  •         Family: Acholeplasmataceae
  • Summary of Invasiveness
  • Ca. Phytoplasma pini’ is a member of phytoplasma 16S rRNA gene RFLP group XXI, subgroup XXI-A. It has been identified in a number of European countries, includ...

  • Principal Source
  • Draft datasheet under review

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Pictures

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PictureTitleCaptionCopyright
Candidatus Phytoplasma pini (pine witches'-broom phytoplasma); symptoms on a pine.
TitleSymptoms
CaptionCandidatus Phytoplasma pini (pine witches'-broom phytoplasma); symptoms on a pine.
Copyright©Jacinta lluch Valero/via flickr - CC BY-SA 2.0
Candidatus Phytoplasma pini (pine witches'-broom phytoplasma); symptoms on a pine.
SymptomsCandidatus Phytoplasma pini (pine witches'-broom phytoplasma); symptoms on a pine.©Jacinta lluch Valero/via flickr - CC BY-SA 2.0

Identity

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Preferred Scientific Name

  • Candidatus Phytoplasma pini Schneider et al. (2005)

Preferred Common Name

  • pine witches'-broom phytoplasma

Summary of Invasiveness

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Ca. Phytoplasma pini’ is a member of phytoplasma 16S rRNA gene RFLP group XXI, subgroup XXI-A. It has been identified in a number of European countries, including Germany, Poland, Lithuania, Spain, Czech Republic and Croatia. Outside of Europe it has been identified in China and Mozambique. A related strain has also been identified in Maryland, USA. In the USA, favourable climatic conditions and wide availability of potential host plants of the phytoplasma, suggest that the potential for spread of ‘Ca. Phytoplasma pini’ could be significant. Host plants include Pinus sylvestrisP. halepensisP. mugoP. banksianaP. nigraP. tabuliformisAbies procera and Tsuga canadensis. Symptoms include the formation of ball-like growths containing dwarfed needles, yellowed or reddish needles and the loss of needles. It is transmitted by insect vectors that are currently unknown.

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

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Phytoplasmas belong to the class Mollicutes, along with other bacteria including members of Mycoplasma, Ureaplasma, Acholeplasma, Spiroplasma and Entomoplasma. Unlike most other members of class Mollicutes, phytoplasmas cannot be reliably isolated in axenic culture (Zhao et al., 2015). Because it has not been possible to isolate phytoplasmas in continued culture, the taxonomic convention of ‘Candidatus Phytoplasma’ taxa has been adopted to refer to phytoplasmas that probably represent distinct species. Thus, a phytoplasma strain whose 16S rRNA gene sequence is <97.5% identical to that of all previously described ‘Candidatus Phytoplasma’ species may be described and named as a new ‘Candidatus Phytoplasma’ species (IRPCM, 2004). To date, 43 ‘Candidatus Phytoplasma’ species have been described (Davis et al., 2017; Miyazaki et al., 2017; Naderali et al., 2017).

Ca. Phytoplasma pini’ is a member of phytoplasma 16S rRNA gene RFLP group XXI, subgroup XXI-A. Based on analysis of 16S rRNA gene sequences from named phytoplasmas, ‘Ca. Phytoplasma pini’ is phylogenetically most closely related to ‘Ca. Phytoplasma castaneae’, reported in diseased trees of Japanese chestnut (Castanea crenata) in Korea (Jung et al., 2002). ‘Ca. Phytoplasma pini’ and ‘Ca. Phytoplasma castaneae’ share 95.1% identity of 16S rRNA gene sequences. The reference strain designated for ‘Ca. Phytoplasma pini’ is strain Pin127SR, found in Pinus halepensis in Spain (Schneider et al., 2005). Unique signature sequences distinguishing ‘Ca. Phytoplasma pini’ from other described ‘Ca. Phytoplasma’ taxa were reported as follows: 5’-GGAAATCTTTCGGGATTTTAGT-3’ and 5’-TCTCAGTGCTTAACGCTGTTCT-3’ (Schneider et al., 2005).

Description

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Phytoplasma cells are pleomorphic, consisting of rounded or filamentous bodies of 200-800 nm in diameter surrounded only by a single trilaminar membrane. Flagellae are absent and the cells lack a rigid cell wall.

Distribution

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Ca. Phytoplasma pini’ has been identified in a number of European countries, including Germany, Poland, Lithuania, Spain, Czech Republic and Croatia (Schneider et al., 2005; Śliwa et al., 2008; Kamińska et al., 2011; Ježic et al., 2013; Valiunas et al., 2015). The occurrence of this species from Germany, Poland and Lithuania to Spain and Croatia is consistent with its possible presence throughout most of Europe. Outside of Europe it has been identified in China (Huang et al., 2011), as a mixed infection with ‘Ca. Phytoplasma palmicola’ in Mozambique (Bila et al., 2015a; Bila et al., 2015b) and as a ‘Ca. Phytoplasma pini’-related strain in Maryland, USA (Costanzo et al., 2016).

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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaPresent, few occurrencesPresent based on regional distribution
-HenanPresent, few occurrences20112010Huang et al., 2011

Africa

MozambiquePresent, few occurrences20152012Bila et al., 2015a

North America

USALocalisedPresent based on regional distribution
-MarylandLocalised2016Costanzo et al., 2016Laurel, MD

Europe

CroatiaPresent, few occurrences2012Ježić et al., 2012
Czech RepublicPresent, few occurrences2011Kaminska et al., 2011
GermanyPresent, few occurrences2005Schneider et al., 2005
LithuaniaPresent, few occurrences2015Valiunas et al., 2015Curonian spit and Varena district
PolandPresent, few occurrencesSliwa et al., 2008; Kaminska and Berniak, 2011; Kaminska et al., 2011
SpainPresent, few occurrences2005Schneider et al., 2005

History of Introduction and Spread

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In 2005, Schneider et al. (2005) described a phytoplasma associated with abnormal shoot proliferation, dwarfing and yellowing or twisting of needles, and in some cases development of ball-like growths, in Scots pine (Pinus sylvestris) in Germany (strain PinG) and Aleppo pine (P. halepensis) in Spain (strains Pin127SR and Pin190S), naming the phytoplasma as a novel taxon, ’Candidatus Phytoplasma pini’. In 2008, Śliwa et al. (2008) reported the presence of a ‘Ca. Phytoplasma pini’-related strain in P. sylvestris trees exhibiting abnormal ball-like growths in Poland and suggested that phytoplasmal infection of conifer trees had existed over an extended period of time. In 2015, Valiunas et al. (2015) reported that trees of P. sylvestris and mountain pine (P. mugo) in the forest of the Curonian Spit of western Lithuania and in forests of southern Lithuania, which exhibited symptoms of proliferation of branching, dwarfed reddish or yellow needles, dried shoots and development of ball-like growths, were infected by ‘Ca. Phytoplasma pini’-related strains belonging to group 16SrXXI, subgroup XXI-A. Of close to 300 trees exhibiting the symptoms of pine bunchy top (PineBT) and sampled by Valiunas et al. (2015), 80% were found to be infected by ‘Ca. Phytoplasma pini’-related strains. In 2016, a ‘Ca. Phytoplasma pini’-related strain was reported in Pinus spp. exhibiting witches’-broom growths in Maryland, USA; this strain appears to represent a lineage that differs from ‘Ca. Phytoplasma pini’ reported in Europe (Costanzo et al., 2016).

Risk of Introduction

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Susceptible species of Pinus, as well as other susceptible gymnosperms, are widespread across the USA. They occur in natural and managed forests, in national and regional parks, in managed residential and commercial landscapes and in ornamental and forest tree nurseries. Regional climatic conditions in the USA are similar to those in regions of Europe where ‘Ca. Phytoplasma pini’ has been reported. The favourable climatic conditions, plus wide availability of potential host plants of the phytoplasma and its unknown insect vector(s), suggest that the potential for spread of ‘Ca. Phytoplasma pini’ across the USA could be significant, particularly if a vector were introduced or if the phytoplasma could be spread by a phloem-feeding insect that is already present in the country.  Furthermore, a ‘Ca. Phytoplasma pini’-related strain has recently been reported in the USA (Costanzo et al., 2016).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial ‑ Natural / Semi-naturalNatural forests Present, no further details

Hosts/Species Affected

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Known hosts of ‘Ca. Phytoplasma pini’ include Pinus sylvestris, P. halepensis, P. mugo, P. banksiana, P. nigra, P. tabuliformis, Abies procera and Tsuga canadensis (Schneider et al., 2005; Śliwa et al., 2008; Kamińska et al., 2011; Valiunas et al., 2015). Hosts of the ‘Ca. Phytoplasma pini’-related strain, member of subgroup 16SrXXI-B, found in Maryland, USA include a tree tentatively identified as mountain pine (Pinus pungens) on the basis of morphology and plastid DNA markers (Costanzo et al., 2016).

Currently, subgroup 16SrI-A ‘Ca. Phytoplasma asteris’-related strains found in diseased pine trees in Lithuania (Valiunas et al., 2015) and a ‘Ca. Phytoplasma pini’-related strain reported in infected pine trees in Maryland, USA (Costanzo et al., 2016), are the only other phytoplasmas found thus far to infect any known plant host of ‘Ca. Phytoplasma pini’. However, other phytoplasmas have been reported in different gymnosperm plants. Kamińska and Śliwa (2010) summarized reports of electron microscopic studies indicating possible infections of coniferous plants in Pinaceae, Taxodiaceae and Cupressaceae. An unidentified Picea abies-infecting phytoplasma belonging to group 16SrIII was reported in Poland (Kamińska and Śliwa. 2010), a subgroup 16SrIX-E ‘Ca. Phytoplasma phoenicium’-related phytoplasma was reported to be associated with witches’-broom disease in western juniper (Juniperus occidentalis) and a subgroup 16SrI-B ‘Ca. Phytoplasma asteris’-related phytoplasma was reported in diseased larch (Larix spp.) in Ukraine (Jomantiene et al., 2011). It seems reasonable to hypothesize that some of these phytoplasmas might be capable of infecting plant hosts of ‘Ca. Phytoplasma pini’ and that ‘Ca. Phytoplasma pini’ might be capable of infecting plants such as P. abies, Juniper spp. and/or larch trees.

Symptoms

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A combination of symptoms can be observed in coniferous plants infected by ‘Ca. Phytoplasma pini’ including the formation of ball-like growths containing dwarfed needles, yellowed or reddish needles and loss of needles.

Symptoms of abnormal plant organogenesis appear to be induced through the action of phytoplasma-produced effector molecules (MacLean et al., 2011; Sugio et al., 2011; Minato et al., 2014) that cause derailment of the normal destiny of apical meristems (Wei et al., 2013).

List of Symptoms/Signs

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SignLife StagesType
Growing point / dieback
Leaves / abnormal forms
Leaves / necrotic areas
Leaves / yellowed or dead
Stems / stunting or rosetting
Stems / witches broom

Biology and Ecology

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In infected plants, phytoplasmas are limited to phloem tissue, mainly if not exclusively inhabiting phloem sieve cells. Natural transmission of phytoplasmas is by phloem-feeding insects. The insect vectors acquire the phytoplasma by feeding in infected phloem tissue. The phytoplasma establishes a systemic infection in the insect and enters the salivary glands, from which phytoplasma cells are then incorporated into saliva and injected into the phloem of a susceptible plant host during subsequent feeding. The minimum incubation period from phytoplasma acquisition by the insect to transmission may vary from 7 to 21 days. The time from inoculation to first appearance of symptoms in an infected plant may be 7 to 21 days in an herbaceous host plant, or perhaps six months to a year in a susceptible tree.

Climate

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ClimateStatusDescriptionRemark
C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C

Means of Movement and Dispersal

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The primary mode of spread of ‘Ca. Phytoplasma pini’ appears to be transmission by insect vector(s) that are currently unknown. Presumably, such vectors could be transported regionally or over long distances on lumber and/or on whole plants. As the phytoplasma is systemically distributed in its plant hosts, it is conceivable that long distance movement could occur through transport of plant material for grafting and by the distribution of ornamental coniferous plants produced by propagation of plant parts, e.g. witches’ broom growths, which are found on naturally infected forest or landscape trees.

Seedborne Aspects

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Transmission of ‘Ca. Phytoplasma pini’ in true seed has not been reported.

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Impact

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Valiunas et al. (2015) have suggested that ‘Ca. Phytoplasma pini’ is negatively impacting the national park area of the Curonian Spit, a UNESCO protected area in Lithuania. Reported infection of 80% of a sample of 300 symptomatic trees (Valiunas et al., 2015) may indicate that the phytoplasma has become widespread in some regions and is possibly responsible for significant damage to pine trees in some forests.

Risk and Impact Factors

Top of page Invasiveness
  • Has a broad native range
  • Abundant in its native range
Impact outcomes
  • Host damage
  • Negatively impacts forestry
  • Threat to/ loss of native species
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Diagnosis

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Candidatus Phytoplasma pini’ is detected through the use of polymerase chain reactions (PCRs). These are designed to amplify a segment of the phytoplasmal 16S rRNA gene that is then subjected to RFLP analysis, which determines 16Sr group and subgroup affiliation, and to nucleotide sequencing for identification (Schneider et al., 2005).

Detection and Inspection

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Phytoplasma taxa cannot be distinguished on the basis of morphological or ultrastructural features. In addition, distinct phytoplasma taxa can induce highly similar or indistinguishable symptoms in a given host plant. Further, a given insect vector species may carry and/or transmit more than one taxon of phytoplasma. Thus, phytoplasmas cannot be distinguished on the basis of host plant infected, symptoms induced in a plant or identity of insect vector(s).  Phytoplasmas are distinguished on the basis of results from analysis of conserved genes, mainly those coding for 16S rRNA.

Similarities to Other Species/Conditions

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Distinct phytoplasma taxa can induce highly similar or indistinguishable symptoms in a given host plant.

Gaps in Knowledge/Research Needs

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Thus far, no insect vector of ‘Ca. Phytoplasma pini’ has been identified. The identities of insect vector(s) of ‘Ca. Phytoplasma pini’ and their feeding habitats, phytoplasma acquisition and transmission patterns, life cycles, natural habitats, alternate plant hosts and migration patterns have not yet been determined. The full geographic distribution of the phytoplasma is probably still unknown.

References

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Bila J, Mondjana A, Samils B, Högberg N, 2015b. Potential novel ‘Candidatus Phytoplasma pini’-related strain associated with coconut lethal yellowing in Mozambique. Phytopathogenic Mollicutes, 5, S59-S60.

Bila, J., Mondjana, A., Samils, B., Högberg, N., 2015. Plant Pathology, 64(3) : Wiley-Blackwell.597-604. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12306/full doi:10.1111/ppa.12306

Costanzo S, Rascoe J, Zhao Y, Davis RE, Nakhla MK, 2016. First report of a new 'Candidatus Phytoplasma pini'-related strain associated with witches'-broom of Pinus spp. in Maryland. Plant Disease, 100(8):1776. http://apsjournals.apsnet.org/loi/pdis

Davis, R. E., Zhao Yan, Wei Wei, Dally, E. L., Lee IngMing, 2017. 'Candidatus Phytoplasma luffae', a novel taxon associated with witches' broom disease of loofah, Luffa aegyptica Mill. International Journal of Systematic and Evolutionary Microbiology, 67(8), 3127-3133. http://ijs.microbiologyresearch.org/content/journal/ijsem doi: 10.1099/ijsem.0.001980

Huang S, Tiwari AK, Rao GP, 2011. ‘Candidatus Phytoplasma pini’ affecting Taxodium distichum var. imbricarium in China. Phytopathogenic Mollicutes, 1(2), 91-94.

IRPCM, 2004. ‘Candidatus Phytoplasma’, a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. International Journal of Systematic and Evolutionary Microbiology, 54, 1243-1255.

Ježic, M., Poljak, I., Šafaric, B., Idžojtic, M., Curkovic-Perica, M., 2013. 'Candidatus Phytoplasma pini' in pine species in Croatia. Journal of Plant Diseases and Protection, 120(4), 160-163. http://www.jpdp-online.com

Jomantiene, R., Valiunas, D., Ivanauskas, A., Urbanaviciene, L., Staniulis, J., Davis, R. E., 2011. Larch is a new host for a group 16SrI, subgroup B, phytoplasma in Ukraine. Bulletin of Insectology, 64(Supplement), S101-S102. http://www.bulletinofinsectology.org/

Jung HeeYoung, Sawayanagi, T., Kakizawa, S., Nishigawa, H., Miyata, S. I., Oshima, K., Ugaki, M., Lee JoonTak, Hibi, T., Namba, S., 2002. 'Candidatus Phytoplasma castaneae', a novel phytoplasma taxon associated with chestnut witches' broom disease. International Journal of Systematic and Evolutionary Microbiology, 52(5), 1543-1549. doi: 10.1099/ijs.0.01980-0

Kaminska M, Berniak H, Obdrzalek J, 2011. New natural host plants of 'Candidatus Phytoplasma pini' in Poland and the Czech Republic. Plant Pathology, 60(6):1023-1029. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3059.2011.02480.x/abstract

Kaminska, M., Berniak, H., 2011. Detection and identification of three 'Candidatus Phytoplasma' species in Picea spp. trees in Poland. Journal of Phytopathology, 159(11/12), 796-798. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0434 doi: 10.1111/j.1439-0434.2011.01842.x

Kaminska, M., Sliwa, H., 2010. Detection of X-disease phytoplasma in Picea abies A. Dietr. tree in Poland. Acta Horticulturae, (No.885), 182-190. http://www.actahort.org/books/885/885_23.htm

MacLean, A. M., Sugio, A., Makarova, O. V., Findlay, K. C., Grieve, V. M., Tóth, R., Nicolaisen, M., Hogenhout, S. A., 2011. Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiology, 157(2), 831-841. http://www.plantphysiol.org/content/157/2/831.full doi: 10.1104/pp.111.181586

Minato, N., Himeno, M., Hoshi, A., Maejima, K., Komatsu, K., Takebayashi, Y., Kasahara, H., Yusa, A., Yamaji, Y., Oshima, K., Kamiya, Y., Namba, S., 2014. The phytoplasmal virulence factor TENGU causes plant sterility by downregulating of the jasmonic acid and auxin pathways. Scientific Reports, 4(7399), srep07399. http://www.nature.com/articles/srep07399

Miyazaki A, Shigaki T, Koinuma H, Iwabuchi N, Rauka GB, Kembu A, Saul J, Watanabe K, Nijo T, Maejima K, Yamaji Y, Namba S, 2017. ‘Candidatus Phytoplasma noviguineense’, a novel taxon associated with Bogia coconut syndrome and banana wilt disease on the island of New Guinea. International Journal of Systematic and Evolutionary Microbiology, 68, 170-175.

Naderali N, Naghmeh Nejat, Ganesan Vadamalai, Davis, R. E., Wei Wei, Harrison, N. A., Kong LihLing, Jugah Kadir, Tan YeeHow, Zhao Yan, 2017. International Journal of Systematic and Evolutionary Microbiology, 67(10) : Microbiology Society.3765-3772. http://ijs.microbiologyresearch.org/content/journal/ijsem doi:10.1099/ijsem.0.002187

Schneider B, Torres E, Martín MP, Schröder M, Behnke HD, Seemüller E, 2005. 'Candidatus Phytoplasma pini', a novel taxon from Pinus silvestris and Pinus halepensis. International Journal of Systematic and Evolutionary Microbiology, 55(1):303-307

Sliwa, H., Kaminska, M., Korszun, S., Adler, P., 2008. Detection of 'Candidatus phytoplasma pini' in Pinus sylvestris trees in Poland. Journal of Phytopathology, 156(2), 88-92. http://www.blackwell-synergy.com/loi/jph doi: 10.1111/j.1439-0434.2007.01335.x

Sugio, A., Kingdom, H. N., MacLean, A. M., Grieve, V. M., Hogenhout, S. A., 2011. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 108(48), E1254-E1263. http://www.pnas.org/content/108/48/E1254.full doi: 10.1073/pnas.1105664108

Valiunas, D., Jomantiene, R., Ivanauskas, A., Urbonaite, I., Sneideris, D., Davis, R. E., 2015. Molecular identification of phytoplasmas infecting diseased pine trees in the UNESCO-protected Curonian Spit of Lithuania. Forests, 6(7), 2469-2483. http://www.mdpi.com/1999-4907/6/7/2469/htm doi: 10.3390/f6072469

Wei, W., Davis, R. E., Nuss, D. L., Zhao, Y., 2013. Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture. Proceedings of the National Academy of Sciences of the United States of America, 110(47), 19149-19154. http://www.pnas.org/content/110/47/19149.full doi: 10.1073/pnas.1318489110

Zhao Y, Davis RE, Wei W, Lee I-M, 2015. Should ‘Candidatus Phytoplasma’ be retained within the order Acholeplasmatales?. International Journal of Systematic and Evolutionary Microbiology, 65, 1075-1082.

Zhao Y, Davis RE, Wei W, Shao J, Jomantiene R, 2014. Phytoplasma Genomes: Evolution Through Mutually Complementary Mechanisms, Gene Loss and Horizontal Acquisition. In: Genomics of Plant-Associated Bacteria, Heidelberg, Berlin, Germany: Springer. 234-271.

Links to Websites

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WebsiteURLComment
Phytoplasma Resource Centerhttps://plantpathology.ba.ars.usda.gov/phytoplasma.html

Principal Source

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Draft datasheet under review

Contributors

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21/07/18 Original text by:

Robert E. Davis, Molecular Plant Pathology Laboratory, Agricultural Research Center, Beltsville, Maryland, USA

Yan Zhao, Molecular Plant Pathology Laboratory, Agricultural Research Center, Beltsville, Maryland, USA

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