Skip to main content
Log in

Response of Prunus species to graft-inoculation by two Iranian strains of almond witches’-broom phytoplasma

  • Original Article
  • Published:
Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Almond witches’-broom (AlmWB) is a serious phytoplasma disease of stone fruits; thus far reported from Iran and Lebanon. In the present study the host range of two Iranian AlmWB phytoplasma strains, known as PEAB and AlKI, were examined through graft-inoculation assay. Two-year-old stone fruit seedlings of almond (three cultivars), peach, plum, Myrobalan plum, apricot and sweet cherry were separately graft-inoculated by scions obtained from symptomatic almond seedlings infected by PEAB or AlKI phytoplasma strains. The presence of phytoplasma in the inoculated seedlings, and the type and development of symptoms were evaluated and recorded monthly over one year. Results showed that both phytoplasma strains could be transmitted to almond (‘Pooya’, ‘Mamaei’ and ‘Talkhe’ cultivars), peach and plum seedlings. The disease symptoms were more obvious in almond cultivars. AlmWB phytoplasma strains could not be detected in the inoculated sweet cherry and the Myrobalan plum seedlings. On the other hand, infection of apricot seedlings could only be detected in seedlings inoculated with the PEAB strain. The homologous of the AYWB SAP11 effector protein, known to play a crucial role in phytoplasma infection and symptom expression, was sequence-analyzed in both PEAB and AlKI strains. The SAP11 nucleotide sequence of AlKI strain was identical to that of the SA213 AlmWB phytoplasma strain from Lebanon. Analysis showed high SAP11 sequence diversity between AlmWB phytoplasmas and phytoplasma strains of other 16Sr groups. Despite poor sequence conservation, the structural features and the motifs of SAP11 protein were conserved between AlmWB and distantly related phytoplasma strains; speculating a similar function for this gene in diverse phytoplasmas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The nucleotide sequence of the SAP11 gene from the AlmWB phytoplasma strains, PEAB and AlKI, identified in this study were deposited in the GenBank under accession numbers ON186619 and ON186620.

References

  • Abbasian M, Salehi M (2010) Reaction of stone fruit cultivars to almond witches’ broom phytoplasma. Iran J Plant Pathol 46:153–160

    Google Scholar 

  • Abou-Jawdah Y, Dakhil H, El-Mehtar S, Lee IM (2003) Almond witches’-broom phytoplasma, a potential threat to almond, peach and nectarine. Can J Plant Pathol 25:28–32

    Article  Google Scholar 

  • Abou-Jawdah Y, Karakashian A, Sobh H, Martini M, Lee IM (2002) An epidemic of almond witches’-broom in Lebanon: classification and phylogenetic relationship of the associated phytoplasma. Plant Dis 86:477–484

    Article  CAS  PubMed  Google Scholar 

  • 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’. Microbiol Res 199:57–66

    Article  CAS  PubMed  Google Scholar 

  • Babaei G, Esmaeilzadeh-Hosseini SA, Shirmardi HA, Bertaccini A (2021) Identification of a 16SrIX‐B Phytoplasma strain associated with Daphne mucronata phyllody in Iran. For Pathol 51:e12703

    Article  Google Scholar 

  • Bertaccini A, Arocha-Rosete Y, Contaldo N, Duduk B, Fiore N, Montano HG, Kube M, Kuo CH, Martini M, Oshima K, Quaglino F(2022) Revision of the ‘Candidatus Phytoplasma’species description guidelines. IJSEM 72:005353

  • Bertaccini A, Lee IM (2018) Phytoplasmas: an update. In: Rao GP, Beratccini A, Fiore N, Liefting LW (eds) Phytoplasmas: plant pathogenic Bacteria-I. Springer, Singapore, pp 1–29

    Google Scholar 

  • Daire X, Clair D, Reinert W, Boudon-Padieu E (1997) Detection and differentiation of grapevine yellows phytoplasmas belonging to the elm yellows group and to the stolbur subgroup by PCR amplification of non-ribosomal DNA. Eur J Plant Pathol 103:507–514

    Article  CAS  Google Scholar 

  • Deng S, Hiruki C (1991) Amplification of 16S rRNA genes from culturable and nonculturable mollicutes. J Microbiol Methods 14:53–61

    Article  CAS  Google Scholar 

  • EPPO (2017) Pest risk analysis for ‘Candidatus Phytoplasma phoenicium’. EPPO, Paris. Available at https://pra.eppo.int/pra/3dc3b492-546f-4ae8-952a-10f02a0fdf8f. Accessed 2 May 2022

  • Gundersen DE, Lee IM (1996) Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathol Mediterr 35:144–151

    CAS  Google Scholar 

  • Hogenhout SA, Oshima K, Ammar ED, Kakizawa S, Kingdom HN, Namba S (2008) Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 9:403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. PNAS 106:6416–6421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwabuchi N, Kitazawa Y, Maejima K, Koinuma H, Miyazaki A, Matsumoto O, Suzuki T, Nijo T, Oshima K, Namba S, Yamaji Y (2020) Functional variation in phyllogen, a phyllody-inducing phytoplasma effector family, attributable to a single amino acid polymorphism. Mol Plant Pathol 21:1322–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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? Mol Plant Pathol 18:435–442

    Article  CAS  PubMed  Google Scholar 

  • Kison H, Seemüller E (2001) Differences in strain virulence of the European stone fruit yellows phytoplasma and susceptibility of stone fruit trees on various rootstocks to this pathogen. J Phytopathol 149:533–541

    Article  CAS  Google Scholar 

  • Lee IM, Bottner-Parker KD, Zhao Y, Bertaccini A, Davis RE (2012) Differentiation and classification of phytoplasmas in the pigeon pea witches’-broom group (16SrIX): an update based on multiple gene sequence analysis. IJSEM 62:2279–2285

    PubMed  Google Scholar 

  • Ludwiczak J, Winski A, Szczepaniak K, Alva V, Dunin-Horkawicz S (2019) DeepCoil—a fast and accurate prediction of coiled-coil domains in protein sequences. Bioinformatics 35:2790–2795

    Article  CAS  PubMed  Google Scholar 

  • Marcone C (2014) Molecular biology and pathogenicity of phytoplasmas. Ann Appl Biol 165:199–221

    Article  CAS  Google Scholar 

  • Lova MM, Quaglino F, Abou-Jawdah Y, Choueiri E, Sobh H, Casati P, Tedeschi R, Alma A, Bianco PA (2011) Identification of new 16SrIX subgroups,-F and-G, among ‘Candidatus Phytoplasma phoenicium’ strains infecting almond, peach and nectarine in Lebanon. Phytopathol Mediterr 50:273–282

    CAS  Google Scholar 

  • 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 Physiol 157:831–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minato N, Himeno M, Hoshi A, Maejima K, Komatsu K, Takebayashi Y, Kasahara H, Yusa A, Yamaji Y, Oshima K, Kamiya Y (2014) The phytoplasmal virulence factor TENGU causes plant sterility by downregulating of the jasmonic acid and auxin pathways. Sci Rep 4:7399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosayyebi N, Mehraban Z, Siampour M, Babaei G, Quaglino F (2021) Multilocus sequence typing and phylogenetic analysis revealed two distinct almond witches’-broom phytoplasma subpopulations in Iran. Ann Appl Biol 179:48–59

    Article  CAS  Google Scholar 

  • Pastore M, Piccirillo P, Simeone AM, Tian J, Paltrinieri S, Bertaccini A (2001) Transmission by patch grafting of ESFY phytoplasma to apricot (Prunus armeniaca L.) and Japanese plum (Prunus salicina Lindl). Acta Hortic 550:339–344

    Article  CAS  Google Scholar 

  • Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Quaglino F, Kube M, Jawhari M, Abou-Jawdah Y, Siewert C, Choueiri E, Sobh H, Casati P, Tedeschi R, Lova MM, Alma A (2015) ‘Candidatus Phytoplasma phoenicium ’associated with almond witches’-broom disease: from draft genome to genetic diversity among strain populations. BMC microbiol 15:148

    Article  PubMed  PubMed Central  Google Scholar 

  • Salehi M, Hosseini SA, Salehi E, Quaglino F, Bianco PA (2020) Peach witches’-broom, an emerging disease associated with ‘Candidatus Phytoplasma phoenicium’and ‘Candidatus Phytoplasma aurantifolia’in Iran. Crop Protec 127:104946

    Article  CAS  Google Scholar 

  • Salehi M, Izadpanah K(1995) Almond brooming. In: Proceedings of the 12th Iranian Plant Protection Congress, Karaj, Iran. p 238

  • Salehi M, Izadpanah K, Heydarnejad J (2006) Characterization of a new almond witches’ broom phytoplasma in Iran. J Phytopathol 154:386–391

    Article  CAS  Google Scholar 

  • Salehi M, Salehi E, Siampour M, Quaglino F, Bianco PA (2018) Apricot yellows associated with ‘Candidatus Phytoplasma phoenicium’ in Iran. Phytopathol Mediterr 57:269–283

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Smart CD, Schneider B, Blomquist CL, Guerra LJ, Harrison NA, Ahrens U, Lorenz KH, Seemüller E, Kirkpatrick BC (1996) Phytoplasma-specific PCR primers based on sequences of the 16S-23S rRNA spacer region. Appl Environ Microbiol 62:2988–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. PNAS 108:E1254–E1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugio A, MacLean AM, Hogenhout SA (2014) The small phytoplasma virulence effector SAP 11 contains distinct domains required for nuclear targeting and CIN-TCP binding and destabilization. New Phytol 202:838–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawidian P, Jawhari M, Sobh H, Bianco P, Abou-Jawdah Y (2018) The potential of grafting with selected stone fruit varieties for management of almond witches’ broom. Phytopathol Mediterr 56:458–469

    Google Scholar 

  • Tedeschi R, Picciau L, Quaglino F, Abou-Jawdah Y, Molino Lova M, Jawhari M, Casati P, Cominetti A, Choueiri E, Abdul‐Nour H, Bianco PA (2015) A cixiid survey for natural potential vectors of ‘Candidatus Phytoplasma phoenicium’ in Lebanon and preliminary transmission trials. Ann Appl Biol 16:372–388

    Article  Google Scholar 

  • Tomkins M, Kliot A, Maree AF, Hogenhout SA (2018) A multi-layered mechanistic modelling approach to understand how effector genes extend beyond phytoplasma to modulate plant hosts, insect vectors and the environment. Curr Opin Plant Biol 44:39–48

    Article  PubMed  Google Scholar 

  • Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A (2015) The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res 43:W401–W407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verdin E, Salar P, Danet JL, Choueiri E, Jreijiri F, El Zammar S, Gelie B, Bove JM, Garnier M (2003) ‘Candidatus Phytoplasma phoenicium’ sp. nov, a novel phytoplasma associated with an emerging lethal disease of almond trees in Lebanon and Iran. IJSEM 53:833–838

    CAS  PubMed  Google Scholar 

  • Weintraub PG, Beanland L (2006) Insect vectors of phytoplasmas. Annu Rev Entomol 51:91–111

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. H. Noorbakhsh for assistance in grafting and rearing stone fruit seedlings.

Funding

This work was funded by Shahrekord University, Shahrekord, Iran.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Majid Siampour.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kabiri, H., Siampour, M. & Babaei, G. Response of Prunus species to graft-inoculation by two Iranian strains of almond witches’-broom phytoplasma. J Plant Pathol 105, 29–37 (2023). https://doi.org/10.1007/s42161-022-01230-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-022-01230-y

Keywords

Navigation