Skip to main content
Log in

Occurrence of ‘Candidatus Phytoplasma omanense’-related strains and other phytoplasmas in Sophora alopecuroides plants showing dwarfing and yellowing

  • Original Paper
  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

Sophora alopecuroides dwarfing and yellowing symptoms were observed at the edge of several Damaneh and Fereydun Shahr (Isfahan province, Iran) fields. Polymerase chain reaction using primers P1/P7 and nested PCR using the same primers followed by R16mF2/R16mR2 and R16F2n/R16R2 primer pairs amplified the 16S ribosomal RNA-encoding gene in all the symptomatic plants tested, but not in the asymptomatic ones. RFLP analysis of R16F2n/R16R2 amplicons with AluI, HaeIII, HhaI, HpaI, HpaII, RsaI, MseI and TaqI restriction enzymes showed profiles referable to 16SrII, 16SrVI, 16SrIX, 16SrXII and 16SrXXIX phytoplasma ribosomal groups indicating also the presence of mixed infection in several samples. The identity percentage and the phylogeny obtained after direct sequencing of selected 16S rRNA-encoding gene sequences (R16F2n/R2 amplicons) from symptomatic S. alopecuroides confirmed the presence of phytoplasma strains related to ‘Candidatus Phytoplasma omanense’ (group 16SrXXIX), ‘Ca. P. australasia’ (group 16SrII), and ‘Ca. P. trifolii’ (16SrVI). Moreover, in a few samples/amplicons, 16SrXII-A, 16SrIX-H, 16SrVI-F and 16SrXXIX-A phytoplasma subgroups were identified by real and virtual RFLP analyses. The other phytoplasmas detected were classified in subgroups 16SrII-D and 16SrVI-A. This is the first report of the presence of 16SrII and 16SrXXIX phytoplasma groups and of mixed infection of phytoplasma strains belonging to groups 16SrII, 16SrVI, 16SrIX, 16SrXII and 16SrXXIX in S. alopecuroides worldwide.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allahverdi T, Rahimian H, Babaeizad V (2014) First report of a ‘Candidatus Phytoplasma solani’ isolate affecting Sophora alopecuroides in Iran. New Dis Rep 30:22

    Article  Google Scholar 

  • Al-Saady NA, Khan AJ, Calari A, Al-Subhi AM, Bertaccini A (2008) ‘Candidatus Phytoplasma omanense’, a phytoplasma associated with witches’ broom of Cassia italica (Mill.) Lam. in Oman. Int J Syst Evol Microbiol 58:461–466

    Article  CAS  PubMed  Google Scholar 

  • Babaie G, Khatabi B, Bayat H, Rastgou M, Hosseini A, Salekdeh GH (2007) Detection and characterization of phytoplasma infecting of ornamental and weed plants in Iran. J Phytopathol 155(6):368–372

    Article  Google Scholar 

  • Bertaccini A, Duduk B (2009) Phytoplasma and phytoplasma diseases: a review of recent research. Phytopathol Mediterr 48:355–378

    CAS  Google Scholar 

  • Bertaccini A, Duduk B, Paltrinieri S, Contaldo N (2014) Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. Am J Plant Sci 5:1763–1788

    Article  Google Scholar 

  • Bisby FA, Buckingham J, Harborne JB (1994) Phytochemical dictionary of the Leguminosae. vol 1. Plants and their constituents. Chapman and Hall, London

  • Chen XF, Liang YC, Chen N, Su WM, Xiao H, Wang X, Zhu XP (2013) Molecular identification of a phytoplasma associated with Sophora root yellows. For Pathol 43:415–421

    Google Scholar 

  • Dehghan H, Salehi M, Khanchezar A, Afshar H (2014) Biological and molecular characterization of a phytoplasma associated with greenhouse cucumber phyllody in Fars province, Iran. J Plant Pathol 50(4):185–186

    Google Scholar 

  • Deng SJ, Hiruki C (1991) Amplification of 16S ribosomal- RNA genes from culturable and non culturable mollicutes. J Microbiol Methods 14:53–61

    Article  CAS  Google Scholar 

  • Duduk B, Tian J, Contaldo N, Fan X, Paltrinieri S, Chen Q, Zhao Q, Bertaccini A (2010) Occurrence of phytoplasmas related to stolbur and to ‘Candidatus Phytoplasma japonicum’ in woody host plants in China. J Phytopathol 158:100–104

    Article  CAS  Google Scholar 

  • Esmaeilzadeh-Hosseini SA, Babaei G, Purmohammadi S, Bertaccini A (2019a) Phytoplasmas infecting greenhouse cucumber in Iran. Phytopathogenic Mollicutes 9(1):31–32

    Article  Google Scholar 

  • Esmaeilzadeh-Hosseini SA, Babaei G, Satta E, Bertaccini A (2019b) New host plants and distribution areas of ‘Candidatus Phytoplasma omanense’-related strains in Iran. Phytopathogenic Mollicutes 9(1):13–14

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Khanchezar A, Shamszadeh M (2011a) The first report of a phytoplasma associated with pot marigold phyllody in Iran. Bull Insectol 64(Supplement):S109–S110

    Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Mirzaie A (2011b) Alternate hosts of alfalfa witches’ broom phytoplasma and winter hosts of its vector Orosius albicinctus in Yazd-Iran. Bull Insectol 64(Supplement):S247–S248

    Google Scholar 

  • Esmailzadeh Hosseini SA, Khodakaramian G, Salehi M, Fani SR, Bolok Yazdi HR, Raoufi D, Jadidi O, Bertaccini A (2015a) Status of alfalfa witches’ broom phytoplasma disease in Iran. Phytopathogenic Mollicutes 5(1-Supplement):S65–S66

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Khodakaramian G, Salehi M, Fani SR, Mirchenari SM, Salehi E, Bertaccini A (2015b) Incidence, distribution and economic importance of alfalfa witches’ broom disease in Sistan-Baluchestan (Iran) and characterization of associated phytoplasma. Phytopathogenic Mollicutes 5(2):84–90

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Khodakaramian G, Mirchenari SM, Bertaccini A (2015c) An up to date status of alfalfa witches’ broom disease in Iran. Phytopathogenic Mollicutes 5(1):9–18

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Mirchenari SM, Tarizeh D, Gholampoor H (2015) First report of a 16SrVI group related phytoplasma associated with cucumber phyllody in a greenhouse in Iran. New Dis Rep 32:5

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Babaee G, Salehi M, Mirchenari SM, Bertaccini A (2016) First report of a ‘Candidatus Phytoplasma phoenicium’-related strain (16SrIX-I) associated with yellowing of Onobrychis viciifolia in Iran. New Dis Rep 34:30

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Khodakaramian G, Salehi M, Bertaccini A (2016) Characterization of 16SrII group phytoplasmas associated with alfalfa (Medicago sativa) witches’ broom disease in diverse areas of Iran. J Crop Prot 5(4):581–590

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Khodakaramian G, Salehi M, Bertaccini A (2016) First report of 16SrVI-A and 16SrXII-A phytoplasmas associated with alfalfa witches’ broom diseases in Iran. J Plant Pathol 98(2):369

    Google Scholar 

  • Esmailzadeh Hosseini SA, Khodakaramian G, Salehi M, Bertaccini A (2016d) Molecular identification and phylogenetic analysis of phytoplasmas associated with alfalfa witches’ broom diseases in the western areas of Iran. Phytopathogenic Mollicutes 6(1):16–22

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Mirchenari SM, Bertaccini A (2016) First report of a 16SrII-D phytoplasma associated with Calendula officinalis phyllody in Iran. New Dis Rep 34:22

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Mirchenari SM, Contaldo N, Paltrinieri S, Bertaccini A (2016f) Occurrence of a ‘Candidatus Phytoplasma omanense’-related strain in a bindweed witches’ broom disease in Iran. Phytopathogenic Mollicutes 6(2):87–92

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Babaie G (2017a) Occurrence and molecular characterization of a 16SrVI-A phytoplasma strain associated with greenhouse cucumber phyllody in Iran. Proceedings of 6th Asian Conference on Plant Pathology, Jeju, South Korea, 232

  • Esmailzadeh Hosseini SA, Salehi M, Babaie G, Mohammadi S, Purmohamadi S, Bertaccini A (2017b) Occurrence and molecular characterization of a ‘Candidatus Phytoplasma omanense’-related strain associated with Prunus persica yellowing and decline in Iran. Proceedings of 6th Asian Conference on Plant Pathology, Jeju, South Korea, 233

  • Esmailzadeh Hosseini SA, Salehi M, Babaie G, Paydar Ardakani A (2017) First report of a 16SrII phytoplasma associated with a witches’ broom disease of Tamarix aphylla in Iran. New Dis Rep 36:22

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Salehi E, Babaie G, Bertaccini A (2017d) Molecular characterization of a new phytoplasma associated with Helianthus annuus phyllody in Iran. Phytopathogenic Mollicutes 7(2):81–85

    Article  Google Scholar 

  • Esmailzadeh Hosseini SA, Salehi M, Babaie G, Bertaccini A (2018) Characterization of a 16SrII subgroup D phytoplasma strain associated with Calendula officinalis phyllody in Iran. 3 Biotech 8(7):295–301

    Article  PubMed  PubMed Central  Google Scholar 

  • Fattahi M, Salehi M, Sharzehi A, Esmailzadeh Hosseini SA (2016) Partial biological and molecular characteristics of a phytoplasma associated with Behshahr (Mazandaran) periwinkle phyllody. Iranian J Plant Pathol 52:135–141

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Ghayeb Zamharir M, Azimi H (2019) Detection and characterisation of a phytoplasma associated with cucumber (Cucumis sativus) regional yellows disease in Iran. Arch Phytopathol Plant Protect 51(15–16):889–893

    Google Scholar 

  • Ghayeb Zamharir M, Taheri P (2017) ‘Candidatus Phytoplasma solani’related strain associated with Babylon willow witches’ broom in central provinces of Iran. Aust Plant Dis Notes, 12

  • Ghayeb Zamharir M, Paltrinieri S, Hajivand S, Taheri M, Bertaccini A (2017) Molecular identification of diverse ‘Candidatus Phytoplasma’ species associated with grapevine decline in Iran. J Phytopathol 165(7–8):407–413

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Jadidi O, Esmailzadeh Hosseini SA, Mirrahimi SR, Salehi M (2017) First report of a 16SrII-D phytoplasma strain associated with Prunus dulcis dieback in Iran. Proceeding of 6th Asian Conference on Plant Pathology, Jeju, South Korea, 211

  • Jamshidi E, Jafarpour B, Rouhani H, Salehi M (2014) Association of members of clover proliferation (16SrVI) and pigeon pea witches’ broom (16SrIX) phytoplasma groups with tomato big bud disease in Iran.  Iranian J Plant Pathol 50:77–89

    Google Scholar 

  • Lee I-M, Gundersen-Rindal DE, Davis RE, Bartoszyk IM (1998) Revised classification scheme of phytoplasmas based on RFLP analyses of 16SrRNA and ribosomal protein gene sequences. Int J Syst Bacteriol 48:1153–1169

    Article  CAS  Google Scholar 

  • Mirchenari SM, Massah A, Zirak L (2015) “Bois noir”: new phytoplasma disease of grapevine in Iran. J Plant Protect Res 55(1):88–93

    Article  CAS  Google Scholar 

  • Mirzaie A, Esmailzadeh Hosseini SA, Jafari-Nodooshan A, Rahimian H (2007) Molecular characterization and potential insect vector of a phytoplasma associated with garden beet witches broom in Yazd, Iran. J Phytopathol 155(4):198–203

    Article  CAS  Google Scholar 

  • Mozafarian V (2008) A dictionary of Iranian plant names. Farhangmoaser Press, Tehran, 596 pp

  • Purmohammadi S, Esmailzadeh Hosseini SA, Gholampoor H, Mirchenari SM (2017) Occurrence of a 16SrVI phytoplasma strain associated with alfalfa witches’ broom disease in Yazd, Iran. P. 31 in proceeding of 2nd International and 10th National Biotechnology Congress of Islamic Republic of Iran. Seed and Plant Improvement Institute, Karaj, Iran

  • Saitou N, Nei M (1987) The neighbour-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA (2016) The first report of a 16SrXII-A Phytoplasma associated with tomato big bud disease in Iran. J Plant Pathol 98(3):677–697

    Google Scholar 

  • Salehi M, Izadpanah K, Siampour M (2007) Characterization of a phytoplasma associated with cabbage yellows in Iran. Plant Dis 91:625–630

    Article  CAS  PubMed  Google Scholar 

  • Salehi M, Haghshenas F, Khanchezar A, Esmailzadeh Hosseini SA (2011) Association of ‘Candidatus Phytoplasma phoenicium’ with GF-677 witches’ broom in Iran. Bull Insectol 64(Supplement):113–114

    Google Scholar 

  • Salehi E, Salehi M, Taghavi SM, Izadpanah K (2014) 16SrII-D Phytoplasma strain associated with tomato witches’ broom in Bushehr province, Iran. J Crop Protect 3(3):377–388

    Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Salehi E (2015) Characterisation of a phytoplasma associated with sunflower phyllody in Fars, Isfahan and Yazd provinces of Iran. New Dis Rep 3:6

    Article  Google Scholar 

  • Salehi M, Siampour M, Esmailzadeh Hosseini SA, Bertaccini A (2015b) Characterization and vector identification of phytoplasmas associated with cucumber and squash phyllody in Iran. Bull Insectol 68(2):311–319

    Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Rasoulpour R, Salehi E, Bertaccini A (2016a) Identification of a phytoplasma associated with pomegranate little leaf disease in Iran. Crop Prot 87:50–54

    Article  CAS  Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Salehi E, Bertaccini A (2016) Molecular and biological characterization of a 16SrII phytoplasma associated with carrot witches’ broom in Iran. J Plant Pathol 98(1):83–90

    Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Salehi E, Bertaccini A (2016c) Genetic diversity and vector transmission of phytoplasmas associated with sesame phyllody in Iran. Folia Microbiol 62(2):99–109

    Article  CAS  Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Salehi E, Bertaccini A (2016d) Occurrence and characterization of a 16SrII-D subgroup phytoplasma associated with parsley witches’ broom disease in Iran. J Phytopathol 164:996–1002 ()

    Article  CAS  Google Scholar 

  • Salehi M, Esmailzadeh Hosseini SA, Salehi E, Bertaccini A (2018) Detection and characterisation of phytoplasma strains associated with field bindweed witches’ broom disease in Iran. Arch Phytopathol Plant Protect 51(15–16):803–813

    Article  CAS  Google Scholar 

  • Schneider B, Seemüller E, Smart CD, Kirkpatrick BC (1995) Phylogenetic classification of plant pathogenic mycoplasma-like organisms or phytoplasmas. In: Tully RS (ed) Molecular and Diagnostic Procedures in Mycoplasmology. Academic, San Diego, pp 369–380

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

  • Yu ZC, Cao Y, Zhang Q, Deng DF, Liu ZY (2012) ‘Candidatus Phytoplasma ziziphi’ associated with Sophora japonica witches’ broom disease in China. J Gen Plant Pathol 78:298–300

  • Zhang YP, Uyemoto JK, Kirkpatrick BC (1998) A small-scale procedure for extracting nucleic acids from woody plants infected with various phytoplasmas for PCR assay. J Virol Methods 71:45–50

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Wei W, Lee I-M, Shao J, Suo X, Davis RE (2009) Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). Int J Syst Evol Microbiol 59:2582–2593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zibadoost S, Rastgou M (2016) Molecular identification of phytoplasmas associated with some weeds in West Azerbaijan province, Iran. Acta Agric Slov 107:129–136

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. A. Esmaeilzadeh-Hosseini.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Esmaeilzadeh-Hosseini, S.A., Satta, E., Babaei, G. et al. Occurrence of ‘Candidatus Phytoplasma omanense’-related strains and other phytoplasmas in Sophora alopecuroides plants showing dwarfing and yellowing. Australasian Plant Pathol. 49, 403–411 (2020). https://doi.org/10.1007/s13313-020-00712-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-020-00712-w

Keywords

Navigation