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Abstract

Phytoplasmas (genus ‘ Phytoplasma’) encompass a group of uncultivated bacteria affecting numerous plant species and causing significant damage in agriculture worldwide. They have a dual parasitic cycle, including colonization of both plant phloem and insect cells. Their genomes are small, diverse, repetitive, prone to rearrangements and harbour transposon-like elements known as potential mobile units (PMUs). In the Euro-Mediterranean region, ‘. P. solani’ is an important species due to its broad range of plant hosts and insect vectors. To provide insights into the genomic diversity of this species, particularly the repertoire of putative effectors and PMUs, this study conducted genome sequencing and analyses of two . P. solani’ strains originating from different plants and transmitted by different insects. Based on assembly, we obtained 19 contigs totalling 656 141 bp for strain STOL and 28 contigs totalling 707 036 bp for strain ST19. The prevalence of repetitive sequences and PMUs contributed to the fragmentation of these draft assemblies. The annotation identified 28 and 26 genes that encode putative secreted proteins in these two strains, respectively, including several homologues of previously characterized phytoplasma effectors. Our comparative analyses further identified species- and strain-specific genes. Frequently, genes that encode putative secreted proteins and effectors were found within PMU-like regions in both genomes. Moreover, strain STOL showed characteristics of a more reduced genome, having fewer PMU-like repetitive elements and genome rearrangements, while strain ST19 exhibited a higher level of sequence divergence in its PMU genes. The high levels of genomic diversity among ‘. P. solani’ strains suggested rapid evolution of this species, which may contribute to its wide host range and adaptability potential. This study provides novel data on the diversification of ‘. P. solani’ genomes. These results provide a foundation for future functional studies of putative effectors and their interactions with host targets, which could facilitate deciphering the pathogenicity strategies of this successful and versatile pathogen.

Funding
This study was supported by the:
  • Academia Sinica
    • Principal Award Recipient: Chih-HorngKuo
  • Hrvatska Zaklada za Znanost (Award IP-2019-04-2469)
    • Principal Award Recipient: MartinaŠeruga Musić
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2025-04-28
2026-03-09

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References

  1. Hogenhout SA, Oshima K, Ammar E-D, Kakizawa S, Kingdom HN et al. Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 2008; 9:403–423 [View Article] [PubMed]
    [Google Scholar]
  2. Namba S. Molecular and biological properties of phytoplasmas. Proc Jpn Acad Ser B Phys Biol Sci 2019; 95:401–418 [View Article] [PubMed]
    [Google Scholar]
  3. Bertaccini A, Arocha-Rosete Y, Contaldo N, Duduk B, Fiore N et al. Revision of the ‘Candidatus Phytoplasma’ species description guidelines. Int J Syst Evol Microbiol 2022; 72:005353 [View Article]
    [Google Scholar]
  4. Wei W, Zhao Y. Phytoplasma taxonomy: nomenclature, classification, and identification. Biology 2022; 11:1119 [View Article] [PubMed]
    [Google Scholar]
  5. Oshima K, Kakizawa S, Nishigawa H, Jung H-Y, Wei W et al. Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet 2004; 36:27–29 [View Article] [PubMed]
    [Google Scholar]
  6. Bai X, Zhang J, Ewing A, Miller SA, Jancso Radek A et al. Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J Bacteriol 2006; 188:3682–3696 [View Article] [PubMed]
    [Google Scholar]
  7. Music MS, Samarzija I, Hogenhout SA, Haryono M, Cho S-T et al. The genome of ‘Candidatus Phytoplasma solani’ strain SA-1 is highly dynamic and prone to adopting foreign sequences. Syst Appl Microbiol 2019; 42:117–127 [View Article] [PubMed]
    [Google Scholar]
  8. Marcone C, Neimark H, Ragozzino A, Lauer U, Seemüller E. Chromosome sizes of phytoplasmas composing major phylogenetic groups and subgroups. Phytopathology 1999; 89:805–810 [View Article] [PubMed]
    [Google Scholar]
  9. Toruño TY, Musić MS, Simi S, Nicolaisen M, Hogenhout SA. Phytoplasma PMU1 exists as linear chromosomal and circular extrachromosomal elements and has enhanced expression in insect vectors compared with plant hosts. Mol Microbiol 2010; 77:1406–1415 [View Article] [PubMed]
    [Google Scholar]
  10. Chung WC, Chen LL, Lo WS, Lin CP, Kuo CH. Comparative analysis of the peanut witches’-broom phytoplasma genome reveals horizontal transfer of potential mobile units and effectors. PLoS One 2013; 8:e62770 [View Article] [PubMed]
    [Google Scholar]
  11. Huang C-T, Cho S-T, Lin Y-C, Tan C-M, Chiu Y-C et al. Comparative genome analysis of “Candidatus Phytoplasma luffae” reveals the influential roles of potential mobile units in phytoplasma evolution. Front Microbiol 2022; 13:773608 [View Article] [PubMed]
    [Google Scholar]
  12. Bai X, Correa VR, Toruño TY, Ammar E-D, Kamoun S et al. AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol Plant Microbe Interact 2009; 22:18–30 [View Article] [PubMed]
    [Google Scholar]
  13. Hoshi A, Oshima K, Kakizawa S, Ishii Y, Ozeki J et al. A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proc Natl Acad Sci USA 2009; 106:6416–6421 [View Article] [PubMed]
    [Google Scholar]
  14. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci USA 2011; 108:E1254–63 [View Article] [PubMed]
    [Google Scholar]
  15. MacLean AM, Sugio A, Makarova OV, Findlay KC, Grieve VM et al. Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiol 2011; 157:831–841 [View Article] [PubMed]
    [Google Scholar]
  16. Maejima K, Iwai R, Himeno M, Komatsu K, Kitazawa Y et al. Recognition of floral homeotic MADS domain transcription factors by a phytoplasmal effector, phyllogen, induces phyllody. Plant J 2014; 78:541–554 [View Article] [PubMed]
    [Google Scholar]
  17. Minato N, Himeno M, Hoshi A, Maejima K, Komatsu K et al. The phytoplasmal virulence factor TENGU causes plant sterility by downregulating of the jasmonic acid and auxin pathways. Sci Rep 2014; 4:7399 [View Article] [PubMed]
    [Google Scholar]
  18. Strohmayer A, Schwarz T, Braun M, Krczal G, Boonrod K. The effect of the anticipated nuclear localization sequence of ‘Candidatus Phytoplasma mali’ SAP11-like protein on localization of the protein and destabilization of TCP transcription factor. Microorganisms 2021; 9:1756 [View Article] [PubMed]
    [Google Scholar]
  19. Zhou J, Ma F, Yao Y, Deng M, Chen M et al. Jujube witches’ broom phytoplasma effectors SJP1 and SJP2 induce lateral bud outgrowth by repressing the ZjBRC1-controlled auxin efflux channel. Plant Cell Environ 2021; 44:3257–3272 [View Article] [PubMed]
    [Google Scholar]
  20. Bai B, Zhang G, Li Y, Wang Y, Sujata S et al. The “Candidatus Phytoplasma tritici” effector SWP12 degrades the transcription factor TaWRKY74 to suppress wheat resistance. Plant J 2022; 112:1473–1488 [View Article] [PubMed]
    [Google Scholar]
  21. Mittelberger C, Hause B, Janik K. The ‘Candidatus Phytoplasma mali’ effector protein SAP11CaPm interacts with MdTCP16, a class II CYC/TB1 transcription factor that is highly expressed during phytoplasma infection. PLoS One 2022; 17:e0272467 [View Article] [PubMed]
    [Google Scholar]
  22. Bai B, Zhang G, Pei B, Song Q, Hao X et al. The function of the phytoplasma effector SWP12 depends on the properties of two key amino acids. J Biol Chem 2023; 299:103052 [View Article] [PubMed]
    [Google Scholar]
  23. Correa Marrero M, Capdevielle S, Huang W, Al-Subhi AM, Busscher M et al. Protein interaction mapping reveals widespread targeting of development-related host transcription factors by phytoplasma effectors. Plant J 2024; 117:1281–1297 [View Article] [PubMed]
    [Google Scholar]
  24. Quaglino F, Zhao Y, Casati P, Bulgari D, Bianco PA et al. Candidatus Phytoplasma solani”, a novel taxon associated with stolbur- and bois noir-related diseases of plants. Int J Syst Evol Microbiol 2013; 63:2879–2894 [View Article] [PubMed]
    [Google Scholar]
  25. Quaglino F, Sanna F, Moussa A, Faccincani M, Passera A et al. Identification and ecology of alternative insect vectors of “Candidatus Phytoplasma solani” to grapevine. Sci Rep 2019; 9:19522 [View Article] [PubMed]
    [Google Scholar]
  26. Šeruga M, Škorić D, Botti S, Paltrinieri S, Juretić N et al. Molecular characterization of a phytoplasma from the aster yellows (16SrI) group naturally infecting Populus nigra L. ‘Italica’ trees in Croatia. For Pathol 2003; 33:113–125 [View Article]
    [Google Scholar]
  27. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  28. Li H. New strategies to improve minimap2 alignment accuracy. Bioinformatics 2021; 37:4572–4574 [View Article] [PubMed]
    [Google Scholar]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  30. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  31. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article] [PubMed]
    [Google Scholar]
  32. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  33. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article] [PubMed]
    [Google Scholar]
  34. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article] [PubMed]
    [Google Scholar]
  35. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580 [View Article] [PubMed]
    [Google Scholar]
  36. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  37. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
    [Google Scholar]
  38. Sun J, Lu F, Luo Y, Bie L, Xu L et al. OrthoVenn3: an integrated platform for exploring and visualizing orthologous data across genomes. Nucleic Acids Res 2023; 51:W397–W403 [View Article] [PubMed]
    [Google Scholar]
  39. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinform 2007; 23:2947–2948 [View Article] [PubMed]
    [Google Scholar]
  40. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  41. Mitrović J, Siewert C, Duduk B, Hecht J, Mölling K et al. Generation and analysis of draft sequences of “stolbur” phytoplasma from multiple displacement amplification templates. J Mol Microbiol Biotechnol 2014; 24:1–11 [View Article] [PubMed]
    [Google Scholar]
  42. Iwabuchi N, Kitazawa Y, Maejima K, Koinuma H, Miyazaki A et al. Functional variation in phyllogen, a phyllody-inducing phytoplasma effector family, attributable to a single amino acid polymorphism. Mol Plant Pathol 2020; 21:1322–1336 [View Article] [PubMed]
    [Google Scholar]
  43. Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K et al. The linear chromosome of the plant-pathogenic mycoplasma “Candidatus Phytoplasma mali”. BMC Genomics 2008; 9:306 [View Article] [PubMed]
    [Google Scholar]
  44. Debonneville C, Mandelli L, Brodard J, Groux R, Roquis D et al. The complete genome of the “flavescence dorée” phytoplasma reveals characteristics of low genome plasticity. Biology 2022; 11:953 [View Article] [PubMed]
    [Google Scholar]
  45. Orlovskis Z, Canale MC, Haryono M, Lopes JRS, Kuo C-H et al. A few sequence polymorphisms among isolates of Maize bushy stunt phytoplasma associate with organ proliferation symptoms of infected maize plants. Ann Bot 2017; 119:869–884 [View Article] [PubMed]
    [Google Scholar]
  46. Jović J, Cvrković T, Mitrović M, Krnjajić S, Petrović A et al. Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. Phytopathology 2009; 99:1053–1061 [View Article] [PubMed]
    [Google Scholar]
  47. Cvrković T, Jović J, Mitrović M, Krstić O, Toševski I. Experimental and molecular evidence of reptalus panzeri as a natural vector of bois noir. Plant Pathol 2014; 63:42–53 [View Article]
    [Google Scholar]
  48. Plavec J, Ivančan G, Škorić D, Foissac X, Šeruga Musić M. Genetically divergent ‘Candidatus Phytoplasma solani’ isolates in croatian vineyard pathosystems suggest complex epidemiological networks. Phytopathol Res 2024; 6:46 [View Article]
    [Google Scholar]
  49. Dermastia M, Tomaž Š, Strah R, Lukan T, Coll A et al. Candidate pathogenicity factor/effector proteins of “Candidatus Phytoplasma solani” modulate plant carbohydrate metabolism, accelerate the ascorbate-glutathione cycle, and induce autophagosomes. Front Plant Sci 2023; 14:1232367 [View Article] [PubMed]
    [Google Scholar]
  50. Pecher P, Moro G, Canale MC, Capdevielle S, Singh A et al. Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impacts development and defense of Arabidopsis versus maize. PLoS Pathog 2019; 15:e1008035 [View Article] [PubMed]
    [Google Scholar]
  51. Drcelic M, Skiljaica A, Polak B, Bauer N, Seruga Music M. Candidatus Phytoplasma solani’ predicted effector SAP11-like alters morphology of transformed arabidopsis plants and interacts with AtTCP2 and AtTCP4 plant transcription factors. Pathogens 2024; 13:893 [View Article] [PubMed]
    [Google Scholar]
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