Phytoplasmas in Poaceae species: a threat to the most important cereal crops in Europe

Abstract

Phytoplasmas are phytopathogenic bacteria from the class Mollicutes. Cereal diseases caused by these microorganisms contribute to serious economic losses. Infected plants change the colour of their aboveground parts and are stunted. Bacteria also damage the root system and cause plant necrosis. The ears are deformed, which leads to sterility and reduced grain yield. The disease can cause on average about 50%, and in some cases up to 90% loss in yield. Wheat, oats and barley are susceptible to phytoplasmas from the ribosomal group 16SrI. Bacteria from ribosomal groups 16SrI and 16SrXII infect maize. Phytoplasmas are transmitted to cereals by insects, mainly species representing the Cicadellidae family, e.g. Psammottetix striatus (L.), Dalbulus maidis (DeLong & Wolcott), Macrosteles laevis (Ribaut) and the Cixiidae family e.g. Reptalus panzeri (Löw). In addition, many studies have suggested that wild Poaceae plants may be a reservoir of phytoplasmas in the environment. The occurrence of diverse phytoplasmas in Poaceae species worldwide indicates an ongoing threat towards cereal crops in Europe.

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References

  1. Acs Z, Jović J, Ember I, Cvrković T, Nagy Z, Talaber C, Gergely L, Toševski I, Kölber M (2011) First report of maize redness disease in Hungary. Bull Insectol 64:229–230

    Google Scholar 

  2. Alvarez E, Mejía J, Contaldo N, Paltrinieri S, Duduk B, Bertaccini A (2014) ‘Candidatus Phytoplasma asteris’ strains associated with oil palm lethal wilt in Colombia. Plant Dis 98(3):311–318. https://doi.org/10.1094/PDIS-12-12-1182-RE

    CAS  PubMed  Google Scholar 

  3. Asudi G, Van den Berg J, Midega C, Schneider B, Seemüller E, Pickett J, Khan Z (2016) Detection, identification, and significance of phytoplasmas in wild grasses in East Africa. Plant Dis 100(1):108–115. https://doi.org/10.1094/PDIS-11-14-1173-RE

    CAS  PubMed  Google Scholar 

  4. Bahar M, Wist T, Bekkaoui D, Hegedus D, Olivier C (2018) Aster leafhopper survival and reproduction, and Aster yellows transmission under static and fluctuating temperatures, using ddPCR for phytoplasma quantification. Sci Rep 8(227):1–9. https://doi.org/10.1038/s41598-017-18437-0

    CAS  Google Scholar 

  5. Bedendo I, Davis R, Dally E (1997) Molecular evidence for the presence of maize bushy stunt phytoplasma in corn in Brazil. Plant Dis 81(8):957. https://doi.org/10.1094/PDIS.1997.81.8.957C

    CAS  PubMed  Google Scholar 

  6. Blanche K, Tran-Nguyen L, Gibb K (2003) Detection, identification and significance of phytoplasmas in grasses in northern Australia. Plant Pathol 52:505–512

    Article  Google Scholar 

  7. Brčák J (1979) Leafhopper and planthopper vectors of plant disease agents in central and southern Europe. In: Maramorosch K, Harris K (eds) Leafhopper vectors and plant disease agents. Academic Press-Elsevier, Cambridge, pp 97–154

    Google Scholar 

  8. Calari A, Contaldo N, Ardizzi S, Bertaccini A (2010) Phytoplasma detection in corn with reddening in Italy. In: Current status and perspectives of phytoplasma disease research and management; Sitges, Spain, pp 5

  9. Caudwell A (1983) L’origine des jaunisses à mycoplasmes (MLO) des plantes et l’exemple des jaunisses de la vigne. Agronomie 3(2):103–111

    Article  Google Scholar 

  10. Chen C, Lee C, Chen M (1972) Mycoplasma-like organisms in Cynodon dactylon and Brachiaria distachya affected by white leaf diseases. Report of the Taiwan Sugar Experiment Station 56:49–55

    Google Scholar 

  11. Chen W, Li Y, Wang Q, Wang N, Wu Y (2014) Comparative genome analysis of wheat blue dwarf phytoplasma, an obligate pathogen that causes wheat blue dwarf disease in China. PLoS One 9(5):1–11. https://doi.org/10.1371/journal.pone.0096436

    CAS  Google Scholar 

  12. Credi R, Terlizzi F, Milanesi L, Bondavalli R, Cavallini G, Montermini A, Dradi D (2006) Wild host plants of stolbur phytoplasma and its vector, Hyalesthes obsoletus, at sites of grapevine bois noir occurrence in Emilia-Romagna, Italy. In Ext. Abstracts 15th meeting ICVG; Stellenbosch, South Africa, pp 182–183

  13. De Oliveira E, Magalhães P, Gomide R, Vasconcelos C, Souza I, Oliveira C, Cruz I, Schaffert R (2002) Growth and nutrition of Mollicute-infected maize. Plant Dis 86(9):945–949

    PubMed  Article  Google Scholar 

  14. De Oliveira E, Santos J, Magalhães P, Cruz I (2007) Maize bushy stunt phytoplasma transmission by Dalbulus maidis is affected by spiroplasma acquisition and environmental conditions. Bull Insectol 60(2):229–230

    Google Scholar 

  15. De Oliveira E, Valiūnas D, Jović J, Bedendo I, Urbanavičienė L, De Oliveira C (2018) Occurrence and epidemiological aspects of Phytoplasmas in cereals. In: Rao G, Bertaccini A, Fiore N, Liefting L (eds) Phytoplasmas: plant pathogenic Bacteria – I. Springer, Berlin, pp 67–89

    Google Scholar 

  16. Drobnjakovic T, Peric P, Marcic D, Picciau L, Alma A, Mitrovic J, Duduk B, Bertaccini A (2010) Leafhoppers and cixiids in phytoplasma-infected carrot fields: species composition and potential phytoplasma vectors. Pesticidi i fitomedicina 25(4):311–318. https://doi.org/10.2298/PIF1004311D

    Google Scholar 

  17. Duduk B, Bertaccini A (2006) Corn with symptoms of reddening: new host of stolbur phytoplasma. Plant Dis 90(10):1313–1319. https://doi.org/10.1094/PD-90-1313

    CAS  PubMed  Google Scholar 

  18. Duduk B, Stepanović J, Yadav A, Rao G (2018) Phytoplasmas in weeds and wild plants. In: Rao G, Bertaccini A, Fiore N, Liefting L (eds) Phytoplasmas: plant pathogenic Bacteria – I. Springer, Berlin, pp 313–345

    Google Scholar 

  19. Ebbert M, Nault L (2001) Survival in Dalbulus leafhopper vectors improves after exposure to maize stunting pathogens. Entomol Exp Appl 100(3):311–324

    Article  Google Scholar 

  20. Elliot S, Adler F, Sabelis M (2003) How virulent should a parasite be to its vector? Ecology 84(10):2568–2574

    Article  Google Scholar 

  21. Fedotina V (1977) Virus und mykoplasmaanlicheorganismen in zellen von hafer, der von der pseudorosettenkrankheit befallen ist. Arch Phytopathol Pfl 3:177–191

    Article  Google Scholar 

  22. Frost K, Willis D, Groves R (2011) Detection and variability of Aster yellows phytoplasma titer in its insect vector, Macrosteles quadrilineatus (Hemiptera: Cicadellidae). J Econ Entomol 104(6):1800–1815. https://doi.org/10.1603/ec11183

    CAS  PubMed  Google Scholar 

  23. Genov N, Mitrović J, Genov M, Duduk B (2014) First report of corn reddening caused by ‘Candidatus Phytoplasma solani’ in Bulgaria. Plant Dis 98(7):991–991. https://doi.org/10.1094/PDIS-12-13-1220-PDN

    CAS  PubMed  Google Scholar 

  24. Grigoryevna V (2015) Phytoplasmatic disease of maize under the conditions of Crimea. Izvestiya Orenburgskogo Gosudarstvennogo Agrarnogo Universiteta 5:14–17

    Google Scholar 

  25. Harrison N (1996) PCR assay for detection of the Phytoplasma associated with maize bushy stunt disease. Plant Dis 80:263–269. https://doi.org/10.1094/PD-80-0263

    CAS  Google Scholar 

  26. Henríquez N, Kenyon L, Quiroz L (1999) Corn stunt complex Mollicutes in Belize. Plant Dis 83(1):77. https://doi.org/10.1094/PDIS.1999.83.1.77B

    PubMed  Google Scholar 

  27. Hibino H, Jonson G, Cruz F (1987) Association of mycoplasma like organisms with rice orange leaf in the Philippines. Plant Dis 71(9):792–794

    Article  Google Scholar 

  28. Hoat T, Quan M, Lan Anh D, Cuong N, Vuong P, Alvarez E, Nguyen T, Wyckhuys K, Paltrinieri S, Pardo J, Mejia J, Thanh N, Dickinson M, Duong C, Kumasaringhe N, Bertaccini A (2015) Phytoplasma diseases on major crops in Vietnam. Phytopathogenic Mollicutes 5:69–70. https://doi.org/10.5958/2249-4677.2015.00029.8

    Google Scholar 

  29. Hodgetts J, Chuquillangui C, Muller G, Arocha Y, Gamarra D, Pinillos O, Velit E, Lozada P, Boa E, Boonham N, Mumford R, Barker I, Dickinson M (2009) Surveys reveal the occurrence of phytoplasmas in plants at different geographical locations in Peru. Ann Appl Biol 155:15–27. https://doi.org/10.1111/j.1744-7348.2009.00316.x

    CAS  Google Scholar 

  30. Hollingsworth C, Atkinson L, Samac D, Larsen J, Motteberg C, Abrahamson M, Glogoza P, MacRae I (2008) Region and field level distributions of Aster yellows phytoplasma in small grain crops. Plant Dis 92(4):623–630. https://doi.org/10.1094/PDIS-92-4-0623

    CAS  PubMed  Google Scholar 

  31. Hoy C, Zhou X, Nault L, Miller S, Styer J (1999) Host plant, phytoplasma, and reproductive status effects on flight behavior of aster leafhopper (Homoptera: Cicadellidae). Ann Entomol Soc Am 92(4):523–528. https://doi.org/10.1093/aesa/92.4.523

    Google Scholar 

  32. Hruska A, Gladstone S, Obando R (1996) Epidemic roller coaster: maize stunt disease in Nicaragua. Am Entomol 42(4):248–252

    Article  Google Scholar 

  33. Jaśkiewicz B, Sułek A (2017) Kierunki zmian produkcji zbóż w Polsce. Roczniki Naukowe Stowarzyszenia Ekonomistów Rolnictwa i Agrobiznesu XIX(1):66–73. https://doi.org/10.5604/01.3001.0009.8340

    Google Scholar 

  34. Jomantiene R, Davis R, Alminaite A, Valiunas D, Jasinskaite R (2002) First report of oat as host of a phytoplasma belonging to group 16SrI, subgroup A. Plant Dis 86(4):443–443. https://doi.org/10.1094/PDIS.2002.86.4.443B

    CAS  PubMed  Google Scholar 

  35. Jović J, Cvrković T, Mitrović M, Krnjanjić S, Petrović A, Redinbaugh M, Pratt R, Hogenhout S, Toševski I (2007) Maize redness in Serbia caused by stolbur phytoplasma is transmitted by Reptalus panzeri. Bull Insectol 60(2):397–398

    Google Scholar 

  36. Jović J, Cvrković T, Mitrović M, Krnjajić S, Petrović A, Redinbaugh M, Pratt R, Hogenhout S, Toševski I (2009) Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. Phytopathology 99(9):1053–1061. https://doi.org/10.1094/PHYTO-99-9-1053

    PubMed  Google Scholar 

  37. Jović J, Cvrković T, Mitrović M, Krnjajić S, Krstić O, Redinbaugh M, Pratt R, Toševski I (2011) Hosts of stolbur phytoplasmas in maize redness affected fields. Bull Insectol 64:155–156

    Google Scholar 

  38. Jung H, Sawayanagi T, Wongkaew P, Kakizawa S, Nishigawa H, Wei W, Oshima K, Miyata S, Ugaki M, Hibi T, Namba S (2003) ‘Candidatus Phytoplasma oryzae’, a novel phytoplasma taxon associated with rice yellow dwarf disease. Int J Syst Evol Microbiol 53(6):1925–1929. https://doi.org/10.1099/ijs.0.02531-0

    CAS  PubMed  Google Scholar 

  39. Junqueira A, Bedendo I, Pascholati S (2004) Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiol Mol Plant Pathol 65(4):181–185. https://doi.org/10.1016/j.pmpp.2005.01.005

    CAS  Google Scholar 

  40. Kastalyeva T, Bogoutdinov D, Bottner-Parker K, Girsova N, Lee I (2016) Diverse phytoplasmas associated with diseases in various crops in Russia - pathogens and vectors. Agric Biol 51(3):367–375. https://doi.org/10.15389/agrobiology.2016.3.367eng

    Google Scholar 

  41. Khanna S, Singh J, Singh R, Kumar P, Rani T, Baranwal V, Sirohi A, Bertaccini A (2015) Evidence of association of a ‘Candidatus Phytoplasma cynodontis’ with Bermuda grass (Cynodon dactylon) and ‘Candidatus Phytoplasma asteris’ with periwinkle (Catharanthus roseus) from western Uttar Pradesh, India. Crop Prot 74:138–144. https://doi.org/10.1016/j.cropro.2015.04.017

    Google Scholar 

  42. Klejdysz T (2013) Piewiki (Hemiptera: Cicadomorpha & Fulgoromorpha) jako składnik szkodliwej entomofauny ważniejszych upraw w Polsce. PhD, Institute of Plant Protection-National Research Institute, Poznań, Poland

  43. Koh L, Yap M, Yik C, Niu S, Wong S (2008) First report of phytoplasma infection of grasses in Singapore. Plant Dis 92(2):317. https://doi.org/10.1094/PDIS-92-2-0317C

    CAS  PubMed  Google Scholar 

  44. Kovačević M, Durić Z, Jović J, Perković G, Lolić B, Hrnčić S, Toševski I, Delić D (2014) First report of stolbur phytoplasma associated with maize redness disease of maize in Bosnia and Herzegovina. Plant Dis 98(3):418. https://doi.org/10.1094/PDIS-04-13-0371-PDN

    PubMed  Google Scholar 

  45. Kumar S, Tiwari A, Holkar S, Duttamajumder S, Rao G (2015) Characterization of a 16SrI-B phytoplasma associated with sugarcane leaf yellows disease in India. Sugar Tech 17:156–161

    CAS  Article  Google Scholar 

  46. Kumarasinghe N, Jones P (2008) Identification of white leaf disease of sugarcane in Sri Lanka. Sugar Tech 3:55–58. https://doi.org/10.1007/bf02945532

    Google Scholar 

  47. Lee I, Hammond R, Gundersen D (1993) Universal amplification and analysis of pathogen 16S rDNA for classification and identification of Mycoplasmalike organisms. Phytopathology 83(8):834–842. https://doi.org/10.1094/Phyto-83-834

    CAS  Google Scholar 

  48. Lee I, Pastore M, Vibio M, Danielli A, Attathom S, Davis R, Bertaccini A (1997) Detection and characterization of a phytoplasma associated with annual blue grass (Poa annua) white leaf disease in southern Italy. Eur J Plant Pathol 103(3):251–254. https://doi.org/10.1023/A:1008697928744

    Google Scholar 

  49. Lee I, Gundersen-Rindal D, Bertaccini A (1998) Phytoplasma: ecology and genomic diversity. Phytopathology 88(12):1359–1366. https://doi.org/10.1094/PHYTO.1998.88.12.1359

    CAS  PubMed  Google Scholar 

  50. Lee I, Gundersen-Rindal D, Davis R, Bottner K, Marcone C, Seemüller E (2004) ‘Candidatus Phytoplasma asteris’, a novel phytoplasma taxon associated with aster yellows and related diseases. Int J Syst Evol Microbiol 54(4):1037–1048. https://doi.org/10.1099/ijs.0.02843-0

    CAS  PubMed  Google Scholar 

  51. Li C, Du Y, Xiang B, Zhang P (2013) First report of the association of a ‘Candidatus Phytoplasma ulmi’ isolate with a witches’ broom disease of reed in China. New Dis Rep 28:13

    CAS  Article  Google Scholar 

  52. Li S, Hao W, Lu G, Huang J, Liu C, Zhou G (2015) Occurrence and identification of a new vector of Rice Orange leaf phytoplasma in South China. Plant Dis 99(11):1483–1487. https://doi.org/10.1094/pdis-12-14-1243-re

    CAS  PubMed  Google Scholar 

  53. Mall S, Kumar S, Jadon V, Rao G (2015) Identification of phytoplasma associated with weeds species in India. Indian Phytopathol 68(4):449–453

    Google Scholar 

  54. Marić A, Kosovac Z (1959) Proučavanje uzroka i štetnosti crvenila kukuruza u Vojvodini. Savremena Poljoprivreda 7:1028–1043

    Google Scholar 

  55. Mitrović J, Smiljković M, Seemüller E, Reinhardt R, Hüttel B, Büttner C, Bertaccini A, Kube M, Duduk B (2015) Differentiation of ‘Candidatus Phytoplasma cynodontis’ based on 16S rRNA and groEL genes and identification of a new subgroup, 16SrXIV-C. Plant Dis 99(11):1578–1583. https://doi.org/10.1094/PDIS-01-15-0061-RE

    CAS  PubMed  Google Scholar 

  56. Mori N, Mitrović J, Smiljković M, Duduk N, Paltrinieri S, Bertaccini A, Duduk B (2013) Hyalesthes obsoletus in Serbia and its role in the epidemiology of corn reddening. Bull Insectol 66(2):245–250

    Google Scholar 

  57. Murtomaa A (1966) Aster yellows-type virus infecting grasses in Finland. Ann Agric Fenn 5:324–333

    Google Scholar 

  58. Naderali N, Nejat N, Vadamalai G, Davis RE, Wei W, Harrison NA, Kong L, Kadir J, Tan YH, Zhao Y (2017) ‘Candidatus Phytoplasma wodyetiae’, a new taxon associated with yellow decline disease of foxtail palm (Wodyetia bifurcata) in Malaysia. Int J Syst Evol Microbiol 67(10):3765–3772

    CAS  PubMed  Article  Google Scholar 

  59. Nault L (1980) Maize bushy stunt and corn stunt: a comparison of disease symptoms, pathogen host ranges, and vectors. Phytopathology 70(7):659–662. https://doi.org/10.1094/Phyto-70-659

    Google Scholar 

  60. Nault L, Gordon D, Gingery R, Brangfute O, Loayza J (1979) Identification of maize viruses and Mollicutes and their potential insect vectors in Peru. Phytopathology 69(8):824–828

    Article  Google Scholar 

  61. Obura E, Masiga D, Midega C, Otim M, Wachira F, Pickett J, Khan Z (2011) Hyparrhenia grass white leaf disease, associated with a 16SrXI phytoplasma, newly reported in Kenya. British Society for Plant Pathology 24:17

    Google Scholar 

  62. Olivier C, Lowery D, Stobbs L (2009) Phytoplasma diseases and their relationships with insect and plant hosts in Canadian horticultural and field crops. Can Entomol 141(5):425–462

    Article  Google Scholar 

  63. Omar A (2016) Association of ‘Candidatus Phytoplasma cynodontis’ with Bermuda grass white leaf disease and its new hosts in Qassim province, Saudi Arabia. J Plant Interact 11(1):101–107. https://doi.org/10.1080/17429145.2016.1196401

    CAS  Google Scholar 

  64. Orlovskis Z, Canale M, Haryono M, Lopes J, Kuo C, Hogenhout S (2017) A few sequence polymorphisms among isolates of maize bushy stunt phytoplasma associate with organ proliferation symptoms of infected maize plants. Ann Bot 119(5):869–884. https://doi.org/10.1093/aob/mcw213

    CAS  PubMed  Google Scholar 

  65. Palermo S, Ember I, Botti S, Elekes M, Alma A, Bertaccini A, Orosz A, Kölber M (2004) Presence of stolbur phytoplasma in Cixiidae in Hungarian vineyards. Vitis 43(4):201–203

    Google Scholar 

  66. Pérez-López E, Olivier C, Luna-Rodríguez M, Rodríguez Y, Iglesias L, Castro-Luna A, Adame-García J, Dumonceaux T (2016) Maize bushy stunt phytoplasma affects native corn at high elevations in Southeast Mexico. Eur J Plant Pathol 145:963–971. https://doi.org/10.1007/s10658-016-0883-0

    CAS  Google Scholar 

  67. Pérez-López E, Wist T, Dumonceaux T, Luna-Rodríguez M, Nordin D, Castro-Luna A, Iglesias-Andreu L, Olivier C (2018) Detection of maize bushy stunt phytoplasma in leafhoppers collected in native corn crops grown at high elevations in Southeast Mexico. Fla Entomol 101(1):12–19. https://doi.org/10.1653/024.101.0104

    Google Scholar 

  68. Purar B, Bekavac G, Jocković D, Toldi Tóth É, Kálmán L, Raspudić E, Dimitrijević M (2009) Corn reddening: occurrence, symptoms and field observations. Cereal Res Commun 37(1):121–129. https://doi.org/10.1556/CRC.37.2009.1.14

    Google Scholar 

  69. Rao G, Srivastava S, Gupta P, Sharma S, Singh A, Singh S, Singh M, Marcone C (2008) Detection of sugarcane grassy shoot phytoplasma infecting sugarcane in India and its phylogenetic relationships to closely related phytoplasmas. Sugar Tech 10(1):74–80. https://doi.org/10.1007/s12355-008-0013-1

    CAS  Google Scholar 

  70. Rao G, Mall S, Singh M, Marcone C (2009) First report of a ‘Candidatus Phytoplasma cynodontis’-related strain (group 16SrXIV) associated with white leaf disease of Dichanthium annulatum in India. Australas Plant Dis Notes 4:56–58

    CAS  Google Scholar 

  71. Rao G, Mall S, Marcone C (2010) ‘Candidatus Phytoplasma cynodontis’ (16SrXIV group) affecting Oplismenus burmannii (Retz.) P. Beauv. and Digitaria sanguinalis (L.) Scop. in India. Australas Plant Dis Notes 5:93–95. https://doi.org/10.1109/MM.1987.305012

    Google Scholar 

  72. Rao G, Mall S, Raj S, Snehi S (2011) Phytoplasma diseases affecting various plant species in India. Acta Phytopathol Entomol Hung 46(1):59–99. https://doi.org/10.1556/APhyt.46.2011.1.7

    CAS  Google Scholar 

  73. Rao G, Prakasha T, Priya M, Thorat V, Kumar M, Mishra A, Yadav A (2017a) First report of association of Candidatus phytoplasma cynodontis (16SrXI-B group) with streak, yellowing, and stunting disease in durum and bread wheat genotypes from Central India. Plant Dis 101(7):1314–1314. https://doi.org/10.1094/PDIS-02-17-0163-PDN

    Google Scholar 

  74. Rao G, Kumar M, Madhupriya S (2017b) First report of ‘Candidatus Phytoplasma asteris’ (16SrI-B subgroup) associated with a maize leaf redness disease in India. Phytopathogenic Mollicutes 7(1):52–56

    Article  Google Scholar 

  75. Rao G, Alvarez E, Yadav A (2018) Phytoplasma diseases of industrial crops. In: Rao G, Bertaccini A, Fiore N, Liefting L (eds) Phytoplasmas: plant pathogenic Bacteria – I. Springer, Berlin, pp 91–121

    Google Scholar 

  76. Reddy A, Jeyarajan R (1988) New weed host for rice yellow dwarf (RYD) pathogen. Int Rice Res New 13:35

    Google Scholar 

  77. Rosete Y, Diallo H, Konan Konan J, Assiri P, Séka K, Daniel M, Toualy M, Koffi E, Daramcoum M, Beugré N, Ouattara W, Kouadjo C, Allou K, Fursy-Rodelec N, Doudjo-Ouattara O, Yankey N, Dery S, Maharaj A, Saleh M, Summerbell R, Contaldo N, Paltrinieri S, Bertaccini A, Scott J (2016) Detection and identification of the coconut lethal yellowing phytoplasma in weeds growing in coconut farms in Côte d’Ivoire. Can J Plant Pathol 38(2):164–173. https://doi.org/10.1080/07060661.2016.1191044

    CAS  Google Scholar 

  78. Salar P, Charenton C, Foissac X, Malembic-Maher S (2013) Multiplication kinetics of Flavescence dorée phytoplasma in broad bean. Effect of phytoplasma strain and temperature. Eur J Plant Pathol 135(2):371–381. https://doi.org/10.1007/s10658-012-0093-3

    Google Scholar 

  79. Salehi M, Izadpanah K, Siampour M, Taghizadeh M (2009) Molecular characterization and transmission of bermuda grass white leaf phytoplasma in Iran. J Plant Pathol 91(3):655–661

    CAS  Google Scholar 

  80. Schneider B, Padovan A, De La Rue S, Eichner R, Davis R, Bernuetz A, Gibb K (1999) Detection and differentiation of phytoplasmas in Australia: an update. Aust J Agric Res 50(3):333–342. https://doi.org/10.1071/A98106

    Google Scholar 

  81. Seemüller E, Marcone C, Lauer U, Ragozzino A, Göschl M (1998) Current status of molecular classification of the phytoplasmas. J Plant Pathol 80(1):3–26

    Google Scholar 

  82. Sunpapao A (2016) Preliminary molecular identification of phytoplasma associated with Axonopus compressus white leaf disease. Songklanakarin J Pl Sci 3(4):40–43

    Google Scholar 

  83. Szendrei Z (2012) The impact of plant associations on Macrosteles quadrilineatus management in carrots. Entomol Exp Appl 143(2):191–198. https://doi.org/10.1111/j.1570-7458.2012.01243.x

    Google Scholar 

  84. Tran-Nguyen L, Blanche K, Egan B, Gibb K (2000) Diversity of phytoplasmas in northern Australian sugarcane and other grasses. Plant Pathol 49:666–679. https://doi.org/10.1046/j.1365-3059.2000.00498.x

    Google Scholar 

  85. Urbanavičiené L, Valiunas D, Davis R (2004) Molecular detection of phytoplasmas in oats, barley, and Triticosecale and their classification based on 16S rRNA gene polymorphisms. Žemės Ūkio Mokslai 3:15–19

    Google Scholar 

  86. Urbanavičiené L, Jomantiené R, Valiunas D, Davis R (2007) Molecular identification of 16SrI-A, 16SrI-B, 16SrI-C, and 16SrI-L subgroups of phytoplasmas in gramineous plants in Lithuania. Bull Insectol 60(2):127–128

    Google Scholar 

  87. Vacke J (1966) Ochrana Rostlin (Praha) 2:79

  88. Valarmathi P, Rabindran R, Velazhahan R, Suresh S, Robin S (2013) First report of Rice orange leaf disease phytoplasma (16SrI) in rice (Oryza sativa) in India. Australas Plant Dis Notes 8(1):141–143. https://doi.org/10.1007/s13314-013-0117-7

    Google Scholar 

  89. Valiunas D, Urbanavičienė L, Jomantienė R, Davis R (2007) Molecular detection, classification and phylogenetic analysis of subgroup 16SrI-C phytoplasmas detected in diseased Poa and Festuca in Lithuania. Biologija 53(2):36–39. https://doi.org/10.6001/biologija.v53i2.733

  90. Viswanathan R (2001) Serodiagnosis of phytoplasmas causing grassy shoot disease in sugarcane. In: Teakle D (ed) Rao G, Ford R, Tosi¢ M. Sugarcane Pathology. Taylor & Francis Group, New Hampshire, pp 209–220

  91. Wei W, Davis R, Lee I, Zhao Y (2007) Computer-simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. Int J Syst Evol Microbiol 57:1855–1867

    CAS  PubMed  Article  Google Scholar 

  92. Win N, Jung H (2012) ‘Candidatus Phytoplasma cynodontis’ associated with white leaf disease of golden beard grass (Chrysopogon acicalatus). Trop Plant Pathol 37(1):76–79

    Google Scholar 

  93. Win N, Lee S, Bertaccini A, Namba S, Jung H (2013) ‘Candidatus Phytoplasma balanitae’ associated with witches’ broom disease of Balanites triflora. Int J Syst Evol Microbiol 63:636–640. https://doi.org/10.1099/ijs.0.041566-0

    CAS  PubMed  Google Scholar 

  94. Wongkaew P, Hanboonsong Y, Sirithorn P, Choosai C, Boonkrong S, Tinnangwattana T, Kitchareonpanya R, Damak S (1997) Differentiation of phytoplasmas associated with sugarcane and gramineous weed white leaf disease and sugarcane grassy shoot disease by RFLP and sequencing. Theor Appl Genet 95(4):660–663. https://doi.org/10.1007/s001220050609

    CAS  Google Scholar 

  95. Wu Y, Hao X, Li Z, Gu P, An F, Xiang J, Wang H, Luo L, Liu J, Xiang Y (2010) Identification of the phytoplasma associated with wheat blue dwarf disease in China. Plant Dis 94(8):977–985. https://doi.org/10.1094/PDIS-94-8-0977

    CAS  PubMed  Google Scholar 

  96. Yadav A, Thorat V, Deokule S, Shouche Y, Prasad D (2017) New subgroup 16SrXI-F phytoplasma strain associated with sugarcane grassy shoot (SCGS) disease in India. Int J Syst Evol Microbiol 67(2):374–378. https://doi.org/10.1099/ijsem.0.001635

    PubMed  Google Scholar 

  97. Zhang R, Li W, Huang Y, Wang X, Shan H, Luo Z, Yin J (2016) Group 16SrXI phytoplasma strains, including subgroup 16SrXI-B and a new subgroup, 16SrXI-D, are associated with sugar cane white leaf. Int J Syst Evol Microbiol 66:487–491. https://doi.org/10.1099/ijsem.0.000712

    CAS  PubMed  Google Scholar 

  98. Zibadoost S, Rastgou M (2016) Molecular identification of phytoplasmas associated with some weeds in West Azarbaijan province, Iran. Acta Agric Slov 107(1):129–136. https://doi.org/10.14720/aas.2016.107.1.13

    CAS  Google Scholar 

  99. Zwolińska A, Klejdysz T, Krawczyk K, Nawrot J (2017) The role of selected Auchenorrhyncha species (Hemiptera: Cicadomorpha & Fulgoromorpha) in a transmission of ‘Candidatus Phytoplasma asteris’ phytoplasma – a causal factor of oilseed rape phyllody. Prog Plant Prot 57(1):5–15. https://doi.org/10.14199/ppp-2017-001

    Google Scholar 

  100. Zwolińska A, Krawczyk K, Borodynko-Filas N, Pospieszny H (2019) Non-crop sources of Rapeseed Phyllody phytoplasma (‘Candidatus Phytoplasma asteris’: 16SrI-B and 16SrI-(B/L)L), and closely related strains. Crop Prot 119:59–68. https://doi.org/10.1016/j.cropro.2018.11.015

    Google Scholar 

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Acknowledgements

The authors would like to thank Dr. Zigmunds Orlovskis for sharing the photograph of symptoms of Maize Bushy Stunt disease.

This work was performed in frame of the PhD research program ‘Innowacyjny Doktorat’ (no. B020/0011/19) financially supported by the Wrocław University of Environmental and Life Sciences.

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Correspondence to Marta Jurga.

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Jurga, M., Zwolińska, A. Phytoplasmas in Poaceae species: a threat to the most important cereal crops in Europe. J Plant Pathol 102, 287–297 (2020). https://doi.org/10.1007/s42161-019-00481-6

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Keywords

  • Phytoplasma
  • Cereals
  • Poaceae
  • Weeds