Phytoplasma Effectors and Pathogenicity Factors

  • Assunta Bertaccini
  • Kenro Oshima
  • Kensaku Maejima
  • Shigetou Namba


For the study and the management of phytoplasma-associated diseases, the most relevant knowledge needed is the one related to their pathogenicity. After the availability of full and draft genome sequences of some of the phytoplasmas, a mining search allowed identifying a number of possible virulence factors. Their possible pathogenic action was verified mainly by their expression in transgenic plants such as Arabidopsis spp. and Nicotiana spp. Several possible pathogenicity factors such as TENGU and SAP11 and/or effector molecules were shown to be related to metabolic and or phenotypic modifications indistinguishable from those present in the phytoplasma-infected plants such as phyllody and witches’ broom. The possible pathogenicity factors or disease effectors studied enclosing extrachromosomal DNAs, phloem structural modifications, and very recently miRNAs are also described.


TENGU SAP11 Phyllody Witches’ broom Disease symptomatology Transgenic plants 


  1. Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nature Revue on Molecular Cell Biology 7, 601–611.CrossRefGoogle Scholar
  2. Alix E, Blanc-Potard AB (2008) Peptide-assisted degradation of the Salmonella MgtC virulence factor. Embo Journal 27, 546–557.PubMedCrossRefGoogle Scholar
  3. Anabestani A, Izadpanah K, Abbà S, Galetto L, Ghorbani A, Palmano S, Siampour M, Veratti F, Marzachì C (2017) Identification of putative effector genes and their transcripts in three strains related to ‘Candidatus Phytoplasma aurantifolia’. Microbiological Research 199, 57–66.PubMedCrossRefGoogle Scholar
  4. Albertazzi G, Milc J, Caffagni A, Francia E, Roncaglia E, Ferrari F, Tagliafico E, Stefani E, Pecchioni N (2009) Gene expression in grapevine cultivars in response to “bois noir” phytoplasma infection. Plant Science 176, 792–804.CrossRefGoogle Scholar
  5. Ammar el D, Fulton D, Bai X, Meulia T, Hogenhout SA (2004) An attachment tip and pili-like structures in insect- and plant-pathogenic spiroplasmas of the class Mollicutes. Archives of Microbiology 181, 97–105.PubMedCrossRefGoogle Scholar
  6. Arashida R, Kakizawa S, Ishii Y, Hoshi A, Jung H-Y, Kagiwada S, Yamaji Y, Oshima K, Namba S (2008) Cloning and characterization of the antigenic membrane protein (Amp) gene and in situ detection of Amp from malformed flowers infected with Japanese hydrangea phyllody phytoplasma. Phytopathology 98, 769–775.PubMedCrossRefGoogle Scholar
  7. Bai X, Zhang J, Ewing A, Miller SA, Jancso Radek A, Shevchenko DV, Tsukerman K, Walunas T, Lapidus A, Campbell JW, Hogenhout SA (2006) Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. Journal of Bacteriology 188, 3682–3696.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bai X, Correa VR, Toruno TY, Ammar el D, Kamoun S, Hogenhout SA (2009) AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Molecular Plant Microbe Interactions 22, 18–30.PubMedCrossRefGoogle Scholar
  9. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: signalP 3.0. Journal of Molecular Biology 340, 783–795.CrossRefGoogle Scholar
  10. Bertaccini A, Duduk B (2009) Phytoplasma and phytoplasma diseases: a review of recent research. Phytopathologia Mediterranea 48, 355–378.Google Scholar
  11. Boutareaud A, Danet J-L, Garnier M, Saillard C (2004) Disruption of a gene predicted to encode a solute binding protein of an ABC transporter reduces transmission of Spiroplasma citri by the leafhopper Circulifer haematoceps. Applied Environmental Microbiology 70, 3960–3967.PubMedCrossRefGoogle Scholar
  12. Cao X, Zhai X, Zhang Y, Cheng Z, Li X, Fan G (2018) Comparative analysis of microRNA expression in three paulownia species with phytoplasma infection. Forests 9, 302.CrossRefGoogle Scholar
  13. Carraro L, Ermacora P, Loi N, Osler R (2004) The recovery phenomenon in apple proliferation-infected apple trees. Journal of Plant Pathology 86, 141–146.Google Scholar
  14. Chang SH, Tan CM, Wu CT, Lin TH, Jiang SY, Liu RC, Tsai MC, Su LW, Yang JY (2018) Alterations of plant architecture and phase transition by the phytoplasma virulence factor SAP11. Journal of Experimental Botany 22, 5389–5401.Google Scholar
  15. Chitarra W, Pagliarani C, Abbà S, Boccacci P, Birello G, Rossi M, Palmano S, Marzachì C, Perrone I, Gambino G (2018) MiRVIT: a novel miRNA database and its application to uncover Vitis responses to “flavescence dorée” infection. Frontiers in Plant Science 9, 1034.Google Scholar
  16. Christensen NM, Axelsen KB, Nicolaisen M, Schulz A (2005) Phytoplasmas and their interactions with hosts. Trends in Plant Science 10, 526–535.PubMedCrossRefGoogle Scholar
  17. Cornelis GR, van Gijsegem F (2000) Assembly and function of type III secretory systems. Annual Revue of Microbiology 54, 735–774.CrossRefGoogle Scholar
  18. Crespi M, Messens E, Caplan AB, van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO Journal 11, 795–804.PubMedCrossRefGoogle Scholar
  19. Davis MJ, Tsai JH, Cox RL, McDaniel LL, Harrison NA (1988) Cloning of the chromosomal and extrachromosomal DNA of the mycoplasma-like organisms that causes maize bushy stunt disease. Molecular Plant Microbe Interaction 4, 295–302.CrossRefGoogle Scholar
  20. Denes AS, Sinha RC (1991) Extrachromosomal DNA elements of plant pathogenic mycoplasma-like organisms. Canadian Journal of Plant Pathology 13, 26–32.CrossRefGoogle Scholar
  21. Denes AS, Sinha RC (1992) Alteration of clover phyllody mycoplasma DNA after in vitro culturing of phyllody diseased clover. Canadian Journal of Plant Pathology 14, 189–196.CrossRefGoogle Scholar
  22. Fernandez FD, Debat HJ, Conci LR (2018) Molecular characterization of effector protein SAP54 in Bellis virescence phytoplasma (16SrIII-J). BioRxiv 411140, doi:
  23. Forest ER, Rümpler F, Gramzow L, Theißen G, Melzer R (2015) Did convergent protein evolution enable phytoplasmas to generate “zombie plants”? Trends in Plant Science 20, 798–806.CrossRefGoogle Scholar
  24. Goodwin P (1983) Molecular-size limit for movement in the symplast of the elodea leaf. Planta 157, 124–130.PubMedCrossRefGoogle Scholar
  25. Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiology and Molecular Biology Revue 67, 277–301.CrossRefGoogle Scholar
  26. Higgins CF (2001) ABC transporters: physiology, structure and mechanism - an overview. Research in Microbiology 152, 205–210.PubMedCrossRefGoogle Scholar
  27. Himeno M, Neriya Y, Minato N, Miura C, Sugawara K, Ishii Y, Yamaji Y, Kakizawa S, Oshima K, Namba S (2011) Unique morphological changes in plant pathogenic phytoplasma-infected petunia flowers are related to transcriptional regulation of floral homeotic genes in an organ-specific manner. Plant Journal 67, 971–979.PubMedCrossRefGoogle Scholar
  28. Himeno M, Kitazawa Y, Yoshida T, Maejima K, Yamaji Y, Oshima K, Namba S (2014) Purple top symptoms are associated with reduction of leaf cell death in phytoplasma-infected plants. Science Reporter 4, 4111.CrossRefGoogle Scholar
  29. Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378–379.PubMedCrossRefGoogle Scholar
  30. Hogenhout SA, Oshima K, Ammar E-D, Kakizawa S, Kingdom HN, Namba S (2008) Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology 9, 403–423.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Hoshi A, Oshima K, Kakizawa S, Ishii Y, Ozeki J, Hashimoto M, Komatsu K, Kagiwada S, Yamaji Y, Namba S (2009) A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proceeding of the National Academy of Science United States of America 106, 6416–6421.CrossRefGoogle Scholar
  32. Hren M, Nikolic P, Rotter A, Blejec A, Terrier N, Ravnikar M, Dermastia M, Gruden K (2009) “Bois noir” phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genomics 10, 460.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309–322.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Janik K, Mithöfer A, Raffeiner M, Stellmach H, Hause B, Schlink K (2017) An effector of apple proliferation phytoplasma targets TCP transcription factors — a generalized virulence strategy of phytoplasma? Molecular Plant Pathology 18, 435–442.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Joshi BD, Berg M, Rogers J., Fletcher J, Melcher U (2005) Sequence comparisons of plasmids pBJS-O of Spiroplasma citri and pSKU146 of S. kunkelii: implications for plasmid evolution. BMC Genomics 6, 175.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Kempers R, van Bel A (1997) Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L have a molecular exclusion limit of at least 10 kDa. Planta 201, 195–201.CrossRefGoogle Scholar
  37. Kitazawa Y, Iwabuchi N, Himeno M, Sasano M, Koinuma H, Nijo T, Tomomitsu T, Yoshida T, Okano Y, Yoshikawa N, Maejima K, Oshima K, Namba S (2017) Phytoplasma-conserved phyllogen proteins induce phyllody across the Plantae by degrading floral MADS domain proteins. Journal of Experimental Botany 68, 2799–2811.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K, Migdoll AM, Reinhardt R, Seemüller E (2008) The linear chromosome of the plant-pathogenic mycoplasma ‘Candidatus Phytoplasma mali’. BMC Genomics 9, 306.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kuboyama T, Huang C-C, Lu X, Sawayanagi T, Kanazawa T, Kagami T, Matsuda I, Tsuchizaki T, Namba S (1998) A plasmid isolated from phytopathogenic onion yellows phytoplasma and its heterogeneity in the pathogenic phytoplasma mutant. Molecular Plant Microbe Interactions 11, 1031–1037.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Langklotz S, Baumann U, Narberhaus F (2012) Structure and function of the bacterial AAA protease FtsH. Molecular Cell Research 1823, 40–48.Google Scholar
  41. Lu Y-T, Cheng K-T, Jiang S-Y, Yang J-Y (2014a) Post-translational cleavage and self-interaction of the phytoplasma effector SAP11. Plant Signalling Behaviour 9, 1–3.CrossRefGoogle Scholar
  42. Lu Y-T, Li M-Y, Cheng K-T, Tan CM, Su L-W, Lin W-Y, Shih HT, Chiou TJ, Yang JY (2014b) Transgenic plants that express the phytoplasma effector SAP11 show altered phosphate starvation and defense responses. Plant Physiology 164, 1456–1469.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Luong TT, Sau K, Roux C, Sau S, Dunman PM, Lee CY (2011) Staphylococcus aureus ClpC divergently regulates capsule via sae and codY in strain Newman but activates capsule via codY in strain UAMS-1 and in strain Newman with repaired saeS. Journal of Bacteriology 193, 686–694.PubMedCrossRefGoogle Scholar
  44. Manes de OCL, Beeckman T, Ritsema T, van Montagu M, Goethals K, Holsters M (2004). Phenotypic alterations in Arabidopsis thaliana plants caused by Rhodococcus fascians infection. Journal of Plant Research 117, 139–145.CrossRefGoogle Scholar
  45. Margaria P, Palmano S (2011) Response of the Vitis vinifera L. cv. Nebbiolo proteome to “flavescence dorée” phytoplasma infection. Proteomics 11, 212–224.PubMedCrossRefGoogle Scholar
  46. MacLean AM, Sugio A, Makarova OV, Findlay KC, Grieve VM, Tóth R, Nicolaisen M, Hogenhout SA (2011) Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiology 157, 831–841.PubMedPubMedCentralCrossRefGoogle Scholar
  47. MacLean AM, Orlovskis Z, Kowitwanich K, Zdziarska AM, Angenent GC, Immink RGH, Hogenhout SA (2014) Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. Plos Biology 12, e1001835.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Maejima K, Iwai R, Himeno M, Komatsu K, Kitazawa Y, Fujita N, Ishikawa K, Fukuoka M, Minato N, Yamaji Y, Oshima K, Namba S (2014) Recognition of floral homeotic MADS domain transcription factors by a phytoplasmal effector, phyllogen, induces phyllody. Plant Journal 78, 541–554.PubMedCrossRefGoogle Scholar
  49. Maejima K, Kitazawa Y, Tomomitsu T, Yusa A, Neriya Y, Himeno M, Yamaji Y, Oshima K, Namba S (2015) Degradation of class E MADS-domain transcription factors in Arabidopsis by a phytoplasmal effector, phyllogen. Plant Signal Behaviour 10, e1042635.CrossRefGoogle Scholar
  50. 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, 7399–7405.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Mori Y, Nishimura T, Koshiba T (2005) Vigorous synthesis of indole-3-acetic acid in the apical very tip leads to a constant basipetal flow of the hormone in maize coleoptiles. Plant Science 168, 467–473.CrossRefGoogle Scholar
  52. Musetti R, Buxa SV, De Marco F, Loschi A, Polizzotto R, Kogel K-H, van Bel AJE (2013) Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Molecular Plant Microbe Interactions 26, 379–386.PubMedCrossRefGoogle Scholar
  53. Nishida H, Sugiyama J (1993) Phylogenetic relationships among Taphrina, Saitoella, and other higher fungi. Molecular Biology Evolution 10, 431–436.PubMedGoogle Scholar
  54. Nakashima K, Hayashi T (1995) Extrachromosomal DNAs of rice yellow dwarf and sugarcane white leaf phytoplasmas. Annals of the Phytopathological Society of Japan 61, 456–462.CrossRefGoogle Scholar
  55. Nakashima K, Hayashi T (1997) Sequence analysis of extrachromosomal DNA of sugarcane white leaf phytoplasma. Annals of the Phytopathological Society of Japan 63, 21–25.CrossRefGoogle Scholar
  56. Nakashima K, Kato S, Iwanami S, Murata N (1991) Cloning and detection of chromosomal and extrachromosomal DNA from mycoplasma-like organisms that cause yellow dwarf disease of rice. Applied and Environmental Microbiology 57, 3570–3575.Google Scholar
  57. Nishigawa H, Miyata SI, Oshima K, Sawayanagi T, Komoto A, Kuboyama T, Matsuda I, Tsuchizaki T, Namba S (2001) In planta expression of a protein encoded by the extrachromosomal DNA of a phytoplasma and related to geminivirus replication proteins. Microbiology 147, 507–513.PubMedCrossRefGoogle Scholar
  58. Nishigawa H, Oshima K, Kakizawa S, Jung HY, Kuboyama T, Miyata S, Ugaki M, Namba S (2002) A plasmid from a non-insect-transmissible line of a phytoplasma lacks two open reading frames that exist in the plasmid from the wild-type line. Gene 298, 195–201.PubMedCrossRefGoogle Scholar
  59. Nishigawa H, Oshima K, Miyata S, Ugaki M, Namba S (2003) Complete set of extrachromosomal DNAs from three pathogenic lines of onion yellows phytoplasma and use of PCR to differentiate each line. Journal of General Plant Pathology 69, 194–198.Google Scholar
  60. Orlovskis Z, Canale M, Haryono M, Lopes J, Kuo C-H, Hogenhout S (2017) A few sequence polymorphisms among isolates of maize bushy stunt phytoplasma associate with organ proliferation symptoms of infected maize plants. Annals of Botany 119, 869–884.PubMedGoogle Scholar
  61. Oshima K, Kakizawa S, Nishigawa H, Kuboyama T, Miyata S, Ugaki M, Namba S (2001a) A plasmid of phytoplasma encodes a unique replication protein having both plasmid- and virus-like domains: clue to viral ancestry or result of virus/plasmid recombination? Virology 285, 270–277.PubMedCrossRefGoogle Scholar
  62. Oshima K, Shiomi T, Kuboyama T, Sawayanagi T, Nishigawa H, Kakizawa S, Miyata S, Ugaki M, Namba S (2001b) Isolation and characterization of derivative lines of the onion yellows phytoplasma that do not cause stunting or phloem hyperplasia. Phytopathology 91, 1024–1029.PubMedCrossRefGoogle Scholar
  63. Oshima K, Kakizawa S, Nishigawa H, Jung H-Y, Wei W, Suzuki S, Arashida R, Nakata D, Miyata S, Ugaki M, Namba S (2004) Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nature Genetics 36, 27–29.PubMedCrossRefGoogle Scholar
  64. Oshima K, Kakizawa S, Arashida R, Ishii Y, Hoshi A, Hayashi Y, Kagiwada S, Namba S (2007) Presence of two glycolytic gene clusters in a severe pathogenic line of ‘Candidatus Phytoplasma asteris’. Molecular Plant Pathology 8, 481–489.PubMedCrossRefGoogle Scholar
  65. Patui S, Bertolini A, Clincon L, Ermacora P, Braidot E, Vianello A, Zancani M (2013) Involvement of plasma membrane peroxidases and oxylipin pathway in the recovery from phytoplasma disease in apple (Malus domestica). Physiology of Plants 148, 200–213.CrossRefGoogle Scholar
  66. Pracros P, Renaudin J, Eveillard S, Mouras A, Hernould M (2006) Tomato flower abnormalities induced by “stolbur” phytoplasma infection are associated with changes of expression of floral development genes. Molecular Plant-Microbe Interactions 19, 62–68.PubMedCrossRefGoogle Scholar
  67. Razin S, Yogev D, Naot Y (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiology and Molecular Biology Revue 62, 1094–1156.Google Scholar
  68. Seemüller E, Schneider B (2007) Differences in virulence and genomic features of strains of ‘Candidatus Phytoplasma mali’, the apple proliferation agent. Phytopathology 97, 964–970.PubMedCrossRefGoogle Scholar
  69. Seemüller E, Kunze L, Schaper U (1984) Colonization behavior of MLO, and symptom expression of proliferation-diseased apple trees and decline-diseased pear trees over a period of several years. Zeitschrift Pflanzenkrankh Pflanzenchutz 91, 525–532.Google Scholar
  70. Seemüller E, Kampmann M, Kiss E, Schneider B (2011) HfIB gene-based phytopathogenic classification of ‘Candidatus Phytoplasma mali’ strains and evidence that strain composition determines virulence in multiply infected apple trees. Molecular Plant-Microbe Interactions 24, 1258–1266.PubMedCrossRefGoogle Scholar
  71. Seemüller E, Sule S, Kube M, Jelkmann W, Schneider B (2013) The AAA plus ATPases and HfIB/FtsH proteases of ‘Candidatus Phytoplasma mali’: phylogenetic diversity, membrane topology, and relationship to strain virulence. Molecular Plant-Microbe Interactions 26, 367–376.PubMedCrossRefGoogle Scholar
  72. Seruga-Music M, Samarzija I, Hogenhout SA, Haryono M, Cho S-T, Kuo C-H (2018) The genome of ‘Candidatus Phytoplasma solani’ strain SA-1 is highly dynamic and prone to adopting foreign sequences. Systematic and Applied Microbiology 42, 117–127.PubMedCrossRefGoogle Scholar
  73. Siewert C, Luge T, Duduk B, Seemüller E, Büttner C, Sauer S, Kube M (2014) Analysis of expressed genes of the bacterium ‘Candidatus Phytoplasma mali’ highlights key features of virulence and metabolism. Plos One 9, e94391.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Snider J, Thibault G, Houry WA (2008) The AAA+ superfamily of functionally diverse proteins. Gene Biology 9, 216.CrossRefGoogle Scholar
  75. Sugawara K, Honma Y, Komatsu K, Himeno M, Oshima K, Namba S (2013) The alteration of plant morphology by small peptides released from the proteolytic processing of the bacterial peptide TENGU. Plant Physiology 162, 2005–201410.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Sugio A, MacLean AM, Kingdom HN, Grieve VM, Manimekalai R, Hogenhout SA (2011) Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annual Revue of Phytopathology 49, 175–195.CrossRefGoogle Scholar
  77. Tanaka J, Sasakawa C (2005) Type IV secretion system in Helicobacter pylori: comparison with bacterial type III secretion apparatus. Tanpakushitsu Kakusan Koso 50, 36–43.PubMedPubMedCentralGoogle Scholar
  78. Timpte C, Wilson AK, Estelle M (1994) The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138, 1239–1249.PubMedPubMedCentralGoogle Scholar
  79. Tran-Nguyen LT, Kube M, Schneider B, Reinhardt R, Gibb KS (2008) Comparative genome analysis of ‘Candidatus Phytoplasma australiense’ (subgroup tuf-Australia I; rp-A) and ‘Ca. Phytoplasma asteris’ strains OY-M and AY-WB. Journal of Bacteriology 190, 3979–3991.PubMedPubMedCentralCrossRefGoogle Scholar
  80. van Melderen L, Aertsen A (2009) Regulation and quality control by Lon-dependent proteolysis. Research in Microbiology 160, 645–651.PubMedCrossRefGoogle Scholar
  81. Wang N, Li Y, Chen W, Yang HZ, Zhang PH, Wu YF (2017) Identification of wheat blue dwarf phytoplasma effectors targeting plant proliferation and defence responses. Plant Pathology 67, 603–609.CrossRefGoogle Scholar
  82. Wang N, Yang H, Yin Z, Liu W, Sun L, Wu Y (2018) Phytoplasma effector SWP1 induces witches’ broom symptom by destabilizing the TCP transcription factor BRANCHED1. Molecular Plant Pathology 19, 2623–2634.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Yang C-Y, Huang Y-H, Lin C-P, Lin Y-Y, Hsu H-C, Wang C-N, Daisy Liu L-Y, Shen B-N, Lin S-S (2015) Micro RNA396-targeted short vegetative phase is required to repress flowering and is related to the development of abnormal flower symptoms by the phyllody symptoms effector. Plant Physiology 168, 1702–1716.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Wei W, Davis RE, Nuss DL, Zhao Y (2013) Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture. Proceedings of the National Academy of Sciences United States of America 110, 19149–19154.CrossRefGoogle Scholar
  85. Zamorano A, Fiore N (2016) Draft genome sequence of 16SrIII-J phytoplasma, a plant pathogenic bacterium with a broad spectrum of hosts. Genome Announcements 4, e00602–16.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Zimmermann MR, Schneider B, Mithöfer A, Reichelt M, Seemüller E, Furch ACU (2015) Implications of ‘Candidatus Phytoplasma mali’ infection on phloem function of apple trees. Journal of Endocytobiosis and Cell Research 26, 67–75.Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Assunta Bertaccini
    • 1
  • Kenro Oshima
    • 2
  • Kensaku Maejima
    • 3
  • Shigetou Namba
    • 3
  1. 1.Department of Agricultural and Food SciencesAlma Mater Studiorum – University of BolognaBolognaItaly
  2. 2.Department of Clinical Plant Science, Faculty of Bioscience and Applied ChemistryHosei UniversityTokyoJapan
  3. 3.Department of Agricultural and Environmental Biology, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan

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