Compilation of primers for the detection and classification of phytoplasmas
DOI:
https://doi.org/10.15517/ma.v29i3.29832Keywords:
Mollicute, Candidatus, genome, PCR.Abstract
Phytoplasmas are phytopathogenic prokaryotes of great importance because they have been linked to numerous diseases around the world. The aim of these research was to present the general characteristics, the size and composition of the genome and the genes and/or regions used as molecular markers for the identification and characterization of phytoplasmas. Among its main hosts are fruit and wood trees, vegetables, cut flowers and weeds, which generate alterations in the hormonal balance producing symptoms such as philodias and virescence. Because its isolation in vitro has not been possible, the detection and characterization has been carried out, mainly, with molecular techniques. In addition, the use of New Generation Sequencing (NGS) has allowed to know the complete genome of some phytoplasmas, as well as the regions and genes that constitute it. In the present bibliographic review, the information generated from the molecular techniques and NGS sequencing is compiled, as well as the primers reported to identify some groups of phytoplasmas.
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Abou-Jawdah, Y., H. Dakhil, S. El-Mehtar, and I.M. Lee. 2003. Almond witches’-broom phytoplasma: a potential threat to almond, peach, and nectarine. Can J. Plant Pathol. 25:28-32.
Ahrens, U., K.H. Lorenz, H. Kison, R. Berges, B. Schneider, and E. Seemüller. 1994. Universal, cluster-specific, and pathogen-specific PCR amplification of 16S rDNA for detection and identification of mycoplasma like organism. IOM Letters 3:250.
Aldaghi, M., S. Massart, S. Roussel, and M.H. Jijakli. 2007. Development of a new probe for specific and sensitive detection of “Candidatus Phytoplasma mali” in inoculated apple trees. Ann. Appl. Biol. 2:251-258. doi:10.1111/j.1744-7348.2007.00171.x.
Andersen, M.T., L.W. Liefting, I. Havukkala, and R.E. Beever. 2013. Comparison of the complete genome sequence of two closely related isolates of ‘Candidatus Phytoplasma australiense’ reveals genome plasticity. BMC Genomics 14:529. doi:10.1186/1471-2164-14-529.
Andersen, M.T., R.D. Newcomb, L.W. Liefting, and R.E. Beever. 2006. Phylogenetic analysis of “Candidatus Phytoplasma australiense” reveals distinct populations in New Zealand. Phytopathology 96:838-845. doi:10.1094/PHYTO-96-0838.
Angelini, E., G.L. Bianchi, L. Filippin, C. Morassutti, and M. Borgo. 2007. A new TaqMan method for the identification of phytoplasmas associated with gravepine yellows by real-time PCR assay. J. Microbiol. Method. 68:613-622. doi:10.1016/j.mimet.2006.11.015.
Arnaud, G., S. Malembic-Maher, P. Salar, P. Bonnet, M. Maixner, C. Marcone, E. Boudon-Padieu, and X. Foissac. 2007. Multilocus sequences typing confirms the close genetic interrelatedness of three distinct Flavescence dorée infecting grapevine and alder in Europe. Appl. Environ. Microbiol. 73:4001-4010. doi:10.1128/AEM.02323-06.
Arya, A., I.S. Shergill, M. Williamson, L. Gommersall, N. Arya, and H.R. Patel. 2005. Basic principles of real-time quantitative PCR. Expert Rev. Mol. Diagn. 2:209-219. doi:10.1586/14737159.5.2.209.
Azadvar, M., and V.K. Baranwal. 2010. Molecular characterization and phylogeny of a phytoplasma associated with phyllody disease of toria (Brassica rapa L. subsp. dichotoma (Roxb.)) in India. Indian J. Virol. 21:133-139. doi:10.1007/s13337-011-0023-6.
Bai, X., J. Zhang, A. Ewing, A.S. Miller, A.J. Radek, D.V. Shevchenko, K. Tsukerman, T. Walunas, A. Lapidus, J.W. Campbell, and S.A. Hogenhout. 2006. Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J. Bacteriology 188:3682-3696. doi:10.1128/JB.188.10.3682–3696.2006.
Bai, X., J. Zhang, I.R. Holford, and S.A. Hogenhout. 2004. Comparative genomics identifies genes shared by distantly related insect-transmitted plant pathogenic mollicutes. FEMS Microbiol. Lett. 235:249-258. doi:10.1016/j.femsle.2004.04.043.
Baric, S., and J. Dalla-Via. 2004. A new approach to apple proliferation detection: a highly sensitive real-time PCR assay. J. Microbiol. Methods. 57:135-145. doi:10.1016/j.mimet.2003.12.009.
Bedendo, I.P., R.E. Davis, and E.L. Dally. 2000. Detection and identification of the maize bushy stunt phytoplasma in corn plants in Brazil using PCR and RFLP. Int. J. Pest Manage. 46:73-76. doi:10.1080/096708700227606.
Bekele, B., J. Hodgetts, J. Tomlinson, N. Boonham, P. Nikolić, P. Swarbrick, and M. Dickinson. 2011. Use of a real-time LAMP isothermal assay for detecting 16SrII and XII phytoplasmas in fruit and weeds of the Ethiopian Rift Valley. Plant Pathol. 60:345-355. doi:10.1111/j.1365-3059.2010.02384.x.
Benson, D.A., M. Cavanaugh, K. Clark, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell, and E.W. Sayers. 2013. GenBank. Nucleic Acids Res. 41:36-42. doi:10.1093/nar/gks1195.
Bertaccini, A. 2007. Phytoplasmas: diversity, taxonomy and epidemiology. Front. Biosci. 12:673-689.
Bertaccini, A., and B. Duduk. 2009. Phytoplasma and phytoplasma diseases: a review of recent research. Phytopathol. Medit. 48:355-378. doi:10.14601/Phytopathol_Mediterr-3300.
Bisognin, C., B. Schneider, H. Salm, M.S. Grando, W. Jarausch, E. Moll, and E. Seemüller. 2008. Apple proliferation resistence in apomictic rootstocks and its relationship to phytoplasma concentration and simple sequence repeat genotypes. J. Bacteriol. 98:153-158. doi:10.1094/PHYTO-98-2-0153.
Chang, S.H., S.T. Cho, Ch.L. Chen, J.Y. Yang, and C.H. Kuo. 2015. Draft genome sequence of a 16SrII-A subgroup phytoplasma associated with purple coneflower (Echinacea purpurea) witches’ broom disease in Taiwan. Genome Announc. 3(6):e01398-15. doi:10.1128/genomeA.01398-15.
Chen, W., Y. Li, Q. Wang, N. Wang, and Y. Wu. 2014. Comparative genome analysis of wheat blue dwarf phytoplasma, an obligate pathogen that causes wheat blue dwarf disease in China. PLoS ONE 9(5):e96436. doi:10.1371/journal.pone.0096436.
Christensen, M.N., M. Nicolaisen, M. Hansen, and A. Schulz. 2004. Distribution of phytoplasmas in infected plants as revealed by real-time PCR and bioimaging. Mol. Plant Microbe Interact. 17:1175-1184. doi:10.1094/MPMI.2004.17.11.1175.
Chung, W.C., L.L. Chen, W.S. Lo, C.P. Lin, and C.H. Kuo. 2013. Comparative analysis of the peanut witches´-broom phytoplasma genome reveals horizontal transfer of potential mobile units and effectors. PLoS ONE 8(4):e62770. doi:10.1371/journal.pone.0062770.
Cimerman, A., D. Pacifico, P. Salar, C. Marzachi, and X. Foissac. 2009. Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the stolbur phytoplasma. Appl. Environ. Microbiol. 75:2951-2957. doi:10.1128/AEM.02613-08.
Daire, X., D. Clair, J. Larrue, and E. Boudon-Padieu. 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. doi:10.1023/A:1008641411025
Danet, J.L., G. Balakishiyeva, A. Cimerman, N. Sauvion, V. Marie-Jeanne, G. Labonne, A. Laviňa, A. Batlle, I. Križanac, D. Škorić, P. Ermacora, Ç.U. Serçe, K. Çağlayan, W. Jarausch, and X. Foissac. 2011. Moltilocus sequences analysis reveals the genetic diversity of European fruit tree phytoplasmas and supports the existence of inter-species recombination. Microbiology 157:438-450. doi10.1099/mic.0.043547-0.
Deng, S., and C. Hiruki. 1991. Amplification of 16S rRNA genes from culturable and nonculturable Mollicutes. J. Microbiol. Meth. 14:53-61. doi:10.1016/0167-7012(91)90007-D.
Dickinson, M. 2015. Loop-Mediated Isothermal Amplification (LAMP) for detection of phytoplasmas in the field. Methods Mol. Biol. 1302:99-111. doi:10.1007/978-1-4939-2620-6_8.
Doi, Y., M. Teranaka, K. Yora, and H. Asuyama. 1967. Mycoplasma-or PLT group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches’ broom, aster yellows, or paulownia witches’ broom. Japan. J. Phytopathol. 33:259-266. doi:10.3186/jjphytopath.33.259.
Fabre, A., J.L. Danet, and X. Foissac. 2011. The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene 472:37-41. doi:10.1016/j.gene.2010.10.012.
Fischer, A., I. Santana-Cruz, L. Wambua, C. Olds, C. Midega, M. Dickinson, P. Kawicha, Z. Khan, D. Masiga, J. Jores, and B. Schneider. 2016. Draft genome sequence of “Candidatus Phytoplasma oryzae” strain Mbita1, the causative agent of Napier Stunt disease in Kenya. Genome Annunc. 4(2):e00297-16. doi:10.1128/genomeA.00297-16.
Foissac, X., and P. Carle. 2017. A draft genome of ‘Candidatus Phytoplasma aurantifolia’ the agent of the witches-broom disease of lime. NCBI, USA. https://www.ncbi.nlm.nih.gov/nuccore/NZ_MWKN01000002.1 (accessed Jul. 2017).
Foissac, X., J.L. Danet, S. Malembic-Maher, P. Salar, D. Šafářová, P. Válová, and M. Navrátil. 2013. Tuf and secY PCR amplification and genotyping of phytoplasmas. Methods Mol. Biol. 938:189-204. doi:10.1007/978-1-62703-089-2_16.
Francois, P., M. Tangomo, J. Hibbs, E.-J. Bonetti, C.C. Boehme, T. Notomi, M.D. Perkins, and J. Schrenzel. 2011. Robustness of a Loop-mediated isothermal amplification reaction for diagnostic applications. FEMS Immunol. Med. Microbiol. 62:41-48. doi:10.1111/j.1574-695X.2011.00785.x.
Fukata, S., S. Kato, K. Yoshida, Y. Mizukami, A. Ishida, J. Ueda, M. Kanbe, and Y. Ishimoto. 2003. Detection of tomato yellow leaf curl virus by loop-mediated isothermal amplification reaction. J. Virol. Methods. 112:35-40. doi:10.1016/S0166-0934(03)00187-3.
Galetto, L., D. Bosco, and C. Marzachi. 2005. Universal and group-specific real-time PCR diagnosis of flavescence doreé (16Sr-V), bois noir (16Sr-XII) and apple proliferation (16Sr-X) phytoplasmas from field-collected plant hosts and insect vectors. Ann. Appl. Biol. 147:191-201. doi:10.1111/j.1744-7348.2005.00030.x.
Gasparich, E.G. 2010. Spiroplasmas and phytoplasmas: Microbes associated with plant hosts. Biologicals Rev. 38:193-203. doi:10.1016/j.biologicals.2009.11.007.
Gibb, K.S., A.C. Padovan, and B.D. Mogen. 1995. Studies on sweet potato little-leaf phytoplasma detected in sweet potato and other plant species grawing in Northern Australia. Mol. Plant. Pathol. 85:169-174. doi:10.1094/Phyto-85-169.
Gundersen, D.E., and I.M. Lee. 1996. Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopath. Medit. 35:144-151.
Gundersen, D.E., I.M. Lee, S.A. Rehner, R.E. Davis, and D.T. Kingsbury. 1994. Phylogeny of mycoplasma like organisms (Phytoplasmas): a basis for their classification. J. Bacteriol. 17:5244-5254.
Gutiérrez-Aguirre, I., N. Rački, T. Dreo, and M. Ravnikar. 2015. Droplet digital PCR for absolute quantification of pathogens. Methods Mol. Biol. 302:331-347. doi:10.1007/978-1-4939-2620-6_24.
Harrison, N.A., R.E. Davis, C. Oropeza, E.E. Helmick, M. Narváez, S. Eden-Green, M. Dollet, and M. Dickinson. 2014. ‘Candidatus Phytoplasma palmicola’, associated with a lethal yellowing-type disease of coconut (Cocos nucifera L.) in Mozambique. Int. J. Syst. Evol. Microbiol. 64:1890-1899. do:10.1099/ijs.0.060053-0.
Harrison, N.A., M. Womack, and M.L. Carpio. 2002. Detection and characterization of a Lethal Yellowing (16SrIV) group phytoplasma in Canary Island date palms affected by lethal decline in Texas. Plant Dis. 86:676-681. doi:10.1094/PDIS.2002.86.6.676.
Hindson, J.B., D.K. Ness, A.D. Masquelier, P. Belgrade, J.N. Heredia, J.A. Makarewicz, J.I. Bright, Y.M. Lucero, L.A. Hiddessen, C.T. Legler, K.T. Kitano, R.M. Hodel, F.J. Petersen, W.P. Wyatt, R.E. Steenblock, H.P. Shah, J.L. Bousse, B.C. Troup, C.J. Mellen, K.D. Wittmann, G.N. Erndt, H.T. Cauley, T.R. Koehler, P.A. So, S. Dube, A. K. Rose, L. Montesclaron, S. Wang, P.D. Stumbo, P.S. Hodges, S. Romine, P.F. Milanovich, E.H. White, F.J. Regan, G. Karlin-Neumann, M.C. Hinson, S. Saxonov, and W.B. Colston. 2011. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal. Chem. 83:8604-8610. doi:10.1021/ac202028g.
Hodgetts, J., T. Ball, N. Boonham, R. Mumford, and M. Dickinson. 2007. Use of terminal restriction fragment length polymorphism (T-RFLP) for identification of phytoplasmas in plants. Plant. Pathol. 56:357-365. doi:10.1111/j.1365-3059.2006.01561.x.
Hodgetts, J., N. Boonham, R. Mumford, N. Harrison, and M. Dickinson. 2008. Phytoplasma phylogenetics based on analysis of secA and 23S rRNA gene sequences for improved resolution of candidate species of ‘Candidatus Phytoplasma’. Int. J. Syst. Evol. Microbiol. 58:1826-1837. doi:10.1099/ijs.0.65668-0.
Hodgetts, J., J. Tomlinson, N. Boonham, I. González-Marín, P. Nikolic, P. Swarbrick, E. N. Yankey, and M. Dickinson. 2011. Development of rapid in-field Loop-mediated isothermal amplification (LAMP) assays for phytoplasmas. Bull. Insectol. 64:S41-S42.
Hogenhout, S.A., and M.Š. Music. 2010. Phytoplasma genomics, from sequencing to comparative and functional genomics: What have we learnt? In: P.G. Weintraub, and P.G. Jones, editors, Phytoplasmas genomes, plant host and vectors. CABI, Wallingford, GBR. p.19-36.
Hren, M., J. Boben, A. Rotter, P. Kralj, K. Gruden, and M. Ravnikar. 2007. Real-time PCR detection systems for flavescence doreé and bois noir phytoplasmas in gravepine: comparison with conventional PCR detection and application in diagnostics. Plant Pathol. 58:785-796. doi:10.1111/j.1365-3059.2007.01688.x.
Ishiie, T., Y. Doi, K. Yora, and H. Asuyama. 1967. Suppressive effects of antibiotics of tetracycline group on symptom development of mulberry dwarf disease. Japan. J. Phytopathol. 33:267-275. doi:10.3186/jjphytopath.33.267.
Kakizawa, S., A. Makino, Y. Ishii, H. Tamaki, and Y. Kamagata. 2014. Draft genome sequence of “Candidatus Phytoplasma asteris” strain OY-V, an unculturable plant-pathogenic bacterium. Genome Announc. 2(5):e00944-14. doi:10.1128/genomeA.00944-14.
Kakizawa, S., K. Oshima, H.Y. Jung, S. Suzuki, H. Nishigawa, R. Arashida, S.I. Miyata, M. Ugaki, H. Kishino, and S. Namba. 2006a. Positive selection acting on a surface membrane protein of the plant-pathogenic phytoplasmas. J. Bacteriol. 188:3424-3428. doi:10.1128/JB.188.9.3424–3428.2006.
Kakizawa, S., K. Oshima, and S. Namba. 2006b. Diversity and functional importance of phytoplasma membrane proteins. Trends Microbiol. 14:254-256. doi:10.1016/j.tim.2006.04.008.
Kogovšek, P., J. Hodgetts, J. Hall, N. Prezelj, P. Nikolić, N. Mahle, R. Lenarčič, A. Rotter, M. Dickinson, N. Boonham, M. Dermastia, and M. Ravnikar. 2015. LAMP assay and rapid sample preparation method for on-site detection of flavescence doreé phytoplasma in grapevine. Plant. Pathol. 64:286-296. doi:10.1111/ppa.12266.
Kollar, A., and E. Seemüller. 1989. Base composition of the DNA of mycoplasma-like organisms associated with various plant diseases. J. Plant Pathol. 127:177-186. doi:10.1111/j.1439-0434.1989.tb01127.x.
Kube, M., B. Schneide, H. Kuhl, T. Dandekar, K. Heitmann, A.M. Migdoll, R. Reinhardt, and E. Seemüller. 2008. The linear chromosome of the plant-pathogenic mycoplasma ‘Candidatus Phytoplasma mali’. BMC Genomics 9:306. doi:10.1186/1471-2164-9-306.
Lee, I.M., A. Bertaccini, M. Vibio, and D.E. Gundersen. 1995. Detection of multiple phytoplasma in perennial fruit trees with decline symptoms in Italy. Phytopathology 85:728-735. doi:10.1094/Phyto-85-728.
Lee, I.M., K.D. Bottner-Parker, Y. Zhao, R.E. Davis, and N.A. Harrison. 2010. Phylogenetic analysis and delineation of phytoplasmas based on secY gene sequences. IJSEMI 60:2887-2897. doi:10.1099/ijs.0.019695-0.
Lee, I.M., R.E. Davis, and D.E. Gundersen-Rindal. 2000. Phytoplasma: Phytopathogenic Mollicutes. Annu. Rev. Microbiol. 54:221-255. doi:10.1146/annurev.micro.54.1.221.
Lee, I.M., E. Dawn, E. Gundersen-Rindal, and A. Bertaccini. 1998a. Phytoplasma: Ecology and genomic diversity. Phytopathology 88:1359-1366. doi:10.1094/PHYTO.1998.88.12.1359.
Lee, I.M., E. Dawn, E. Gundersen-Rindal, R.E. Davis, and I.M. Bartoszyk. 1998b. Revised classification scheme of phtyoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. Int. J. Syst. Bacteriol. 48:1153-1169.
Lee, I.M., D.E. Gundersen, R.W. Hammond, and R.E. Davis. 1994. Use of mycoplasma organism (MLO) group-specific oligonucleotide primers for nested-PCR assays to detected Mixed-MLO infections in a single host plant. Mol. Plant Pathol. 84:559-566. doi:10.1094/Phyto-84-559.
Lee, I.M., D.E. Gundersen-Rindal, R.E. Davis, K.D. Bottner, C. Marcone, and E. Seemüller. 2004a. ‘Candidatus Phytoplasma asteris’, a novel phytoplasma taxon associated with aster yellows and related diseases. Int. J. Syst. Evol. Microbiol. 54:1037-1048. doi: 10.1099/ijs.0.02843-0.
Lee, I.M., R.W. Hammond, R.E. Davis, and D.E. Gundersen. 1993. Universal amplification and analysis of pathogen 16SrDNA for classification and identification of mycoplasmalike organisms. Mol. Plant Pathol. 83:834-842.
Lee, I.M., M. Martini, C. Marcone, and S.F. Zhu. 2004b. Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of ‘Candidatus Phytoplasma ulmi’ for the phytoplasma associated with elm yellows. Int. J. Syst. Evol. Microbiol. 54:337-47. doi:10.1099/ijs.0.02697-0.
Lee, I.M., J. Shao, K.D. Bottner-Parker, D. E. Gundersen-Rindal, Y. Zhao, and R.E. Davis. 2015. Draft genome sequence of “Candidatus Phytoplasma pruni” strain CX, a plant-pathogenic bacterium. Genome Announc. 3(5):e01117-15. doi:10.1128/genomeA.01117-15.
Lee, I.M., Y. Zhao, and K.D. Bottner. 2006. SecY gene sequence analysis for finer differentiation of diverse strains in the aster yellows phytoplasma group. Mol. Cell. Probes. 20: 87-91. doi:10.1016/j.mcp.2005.10.001.
Lim, O.P., and B.B. Sears. 1992. Evolutionary relationships of a plant-pathogenic mycoplasmalike organism and Acholeplasma laidlawii deduced from two ribosomal protein gene sequences. J. Bacteriol. 8:2606-2611.
Lorenz, K.H., B. Schneider, U. Ahrens, and E. Seemüller. 1995. Detection of the apple proliferation and pear decline phytoplasmas by PCR amplification of ribosomal and nonribosomal DNA. Phytopathology 85:771-776. doi:10.1094/Phyto-85-771.
Makarova, O., N. Contaldo, S. Paltrinieri, A. Bertaccini, H. Nyskjold, and M. Nicolaisen. 2013. DNA bar-coding for phytoplasma identification. Methods Mol. Biol. 938:301-17. doi:10.1007/978-1-62703-089-2_26.
Malembic-Maher, S., F. Constable, A. Cimerman, G. Arnaud, P. Carle, X. Foissac, and E. Boudon-Padieu. 2008. A chromosome map of the Flavescence dorée phytoplasma. Microbiology 154:1454-1463. doi:10.1099/mic.0.2007/013888-0.
Marcone, C., I.M. Lee, R.E. Davis, A. Ragozzino, and E. Seemüller. 2000. Classification of aster yellows-group phytoplasmas based on combined analyses of rRNA and tuf gene sequences. Int. J. Syst. Evol. Microbiol. 50:1703-1713. doi:10.1099/00207713-50-5-1703.
Marcone, C., H. Neimark, A. Ragozzino, U. Laurer, and E. Seemüller. 1999. Chromosome size of phytoplasmas composing major phylogenetic groups and subgroups. Phytopathology 89:805-810. doi:10.1094/PHYTO.1999.89.9.805
Martini, M., I.M. Lee, K.D. Bottner, Y. Zhao, S. Botti, A. Bertaccini, N.A. Harrison, L. Carraro, C. Marcone, A.J. Khan, and R. Osler. 2007. Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. Int. J. Syst. Evol. Microbiol. 57:2037-2051. doi:10.1099/ijs.0.65013-0.
Mehle, N., T. Dreo, and M. Ravnikar. 2014. Quantitative analysis of “flavescence doreé” phytoplasma with droplet digital PCR. Indian J. Pathol. Microbiol. 4:9-15. doi:10.5958/2249-4677.2014.00576.3.
Mitrović, J., S. Kakizawa, B. Duduk, K. Oshima, S. Namba, and A. Bertaccini. 2011. The groEL gene as an additional marker for finer differentiation of “Candidatus Phytoplasma asteris” – related strains. Ann. Appl. Biol. 159:41-48. doi:10.1111/j.1744-7348.2011.00472.x.
Mitrović, J., C. Siewert, B. Duduk, J. Hecht, K. Mölling, F. Broecker, P. Beyerlein, C. Büttner, A. Bertaccini, and M. Kube. 2014. Generation and analysis of draft sequences of ‘stolbur’ phytoplasma from multiple displacement amplification templates. J. Mol. Microbiol. Biotechnol. 24:1-11. doi:10.1159/000353904.
Mpunami, A.A., A. Tymon, P. Jones, and M.J. Dickinson. 1999. Genetic diversity in the coconut lethal yellowing disease phytoplasmas of East Africa. Plant Pathol. 48:109-114. doi:10.1046/j.1365-3059.1999.00314.x.
Musić, Š.M., M. Krajačić, and D. Škorić. 2008. The use of SSCP analysis in the assessment of phytoplasma gene variability. J. Microbiol. Meth. 73:69-72. doi:10.1016/j.mimet.2008.02.003.
Namba, S., S. Kato, S. Iwanami, H. Oyaizu, H. Shiozawa, and T. Tsuchizaki. 1993. Detection and differentiation of plant-pathogenic mycoplasmalike organisms using Polymerase Chain Reaction. Phytopathology 83:786-791. doi:10.1094/Phyto-83-786.
Neimark, H., and B.C. Kirkpatrick. 1993. Isolation and characterization of full-length chromosomes from non-culturable plant-pathogenic Mycoplasma-like organisms. Mol. Microbiol. 7:21-8. doi:10.1111/j.1365-2958.1993.tb01093.x.
Nejat, N., and G. Vadamalai. 2013. Diagnostic techniques for detection of phytoplasma diseases: past and present. J. Plant Dis. Protect. 120:16-25. doi:10.1007/BF03356449.
Nie, X. 2005. Reverse transcription loop-mediated isothermal amplification of DNA for detection of potato virus Y. Plant Dis. 89:605-610. doi:10.1094/PD-89-0605.
Niu, J.H., H. Juan, Q.X. Guo, C.L. Chen, X.Y. Wang, Q. Liu, and Y.D. Guo. 2012. Evaluation of loop-mediated isothermal amplification (LAMP) assays based on 5S rDNA-IGS2 regions for detecting Meloidogyne enterolobii. Plant Pathol. 61:809-819. doi:10.1111/j.1365-3059.2011.02562.x.
Obura, E., D. Masiga, F. Wachira, B. Gurja, and R.Z. Kha. 2011. Detection of phytoplasma by loop-mediated isothermal amplification of DNA (LAMP). J. Microbiol. Meth. 84:312-16. doi:10.1016/j.mimet.2010.12.011.
Orlovskis, Z., M.C. Canale, M. Haryono, J.R.S. Lopes, C.H. Kuo, and S.A. Hogenhout. 2016. Complete genome sequence of maize bushy stunt phytoplasma M3. Institute of Plant and Microbial Biology, Academia Sinica, 128 Sec. 2, Academia Rd, Taipei 11529, Taiwan. NCBI, USA. https://www.ncbi.nlm.nih.gov/genome/annotation_prok/ (consultado en jun. 2017).
Oshima, K., S. Kakizawa, H. Nishigawa, H.Y. Jung, W. Wei, S. Suzuki, R. Arashida, D. Nakata, S. Miyata, M. Ugaki, and S. Namba. 2004. Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nature Gen. 36:27-29. doi:10.1038/ng1277.
Oshima, K., S.I. Miyata, T. Sawayanagi, S. Kakizawa, H. Nishigawa, H.Y. Jung, K.I. Furuki, M. Yanazaki, S. Suzuki, W. Wei, T. Kuboyama, M. Ugaki, and S. Namba. 2002. Minimal set of metabolic pathways suggested from the genome of Onion Yellows Phytoplasma. J. Gen. Plant. Pathol. 68:225-236. doi:10.1007/PL00013081.
Pacifico, D., L. Galetto, M. Rashidi, S. Abbà, S. Palmano, G. Firrao, D. Bosco, and C. Marzachì. 2015. Decreasing global transcript levels over time suggest that phytoplasma cells enter stationary phase during plant and insect colonization. Appl. Environ. Microbiol. 81:2591-2602. doi:10.1128/AEM.03096-14.
Padovan, A.C., K.S. Gibb, A. Bertaccini, M. Vibio, R.E. Bonfigliolo, P.A. Magarey, and B.B. Sears. 1995. Molecular detection of the Australian grapevine yellows phytoplasma and comparison with grapevine yellows phytoplasma from Italy. Austr. J. Grape Wine Res. 1:25-31. doi:10.1111/j.1755-0238.1995.tb00074.x.
Palmano, S., and G. Firrao. 2000. Diversity of phytoplasmas isolated from insects, determined by a DNA heteroduplex mobility assay and a length polymorphism of the 16S y 23S rDNA spacer region analysis. J. Appl. Microbiol. 89:744-750. doi:10.1046/j.1365-2672.2000.01172.x
Pérez-López, E., D. Rodríguez-Marínez, C.Y. Olivier, M. Luna-Rodríguez, and T.J. Dumonceaux. 2017. Molecular diagnostic assays based on cpn60 UT sequences reveal the geographic distribution of subgrup 16SrXII-(A/I)I phytoplasma in Mexico. Sci. Rep. 7:1-14. doi:10.1038/s41598-017-00895-1.
Pinheiro, B.L., A.V. Coleman, M.C. Hidson, J. Herrmann, J.B. Hindson, S. Bhat, and R.K. Emslie. 2012. Evaluation of a droplet digital polymerase chain reaction format for DNA copy number quantification. Anal. Chem. 84:1003-1011. doi:10.1021/ac202578x.
Quaglino, F., M. Kube, Y. Abou-Jawdah, C. Siewert, E. Choueire, H. Sobh, P. Casati, R. Tedeschi, M.M. Lova, A. Alma, and A.P. Bianco. 2015. ‘Candidatus Phytoplasma phoenicium’ associated with almond witches’-broom disease: from draft genome to genetic diversity among strain populations. BMC Microbiol. 15:148. doi:10.1186/s12866-015-0487-4.
Ravindran, A., J. Levy, E. Pierson, and D.C. Gross. 2012. Development of a Loop-Mediated Isothermal Amplification Procedure as a sensitive and rapid method for detection of ‘Candidatus Liberibacter solanacearum’ in potatoes and psyllids. Phytopathology 112:899-907. doi:10.1094/PHYTO-03-12-0055-R.
Razin, S., D. Yogev, and Y. Naot. 1998. Molecular biology and pathogenicity of Mycoplasmas. Microbiol. Mol. Biol. Rev. 62:1094-1156.
Reveles-Torres, L.R., R. Velásquez-Valle, y J.A. Mauricio-Castillo. 2014. Fitoplasmas: otros agentes fitopatógenos. Folleto Técnico No. 56. INIFAP, México D.F., MEX.
Saccardo, F., M. Martini, S. Palmano, P. Ermacora, M. Scortichini, N. Loi, and G. Firrao. 2012. Genome drafts of four phytoplasma strains of the ribosomal group 16SrIII. Microbiology 158:2805-2814. doi:10.1099/mic.0.061432-0.
Saracco, P., D. Bosco, F. Veratti, and C. Marzachì. 2006. Quantification over time of chrysanthemum yellows phytoplasma (16Sr-I) in leaves and roots of the host plant Chrusanthemun carinatum (Schousboe) following inoculation with its insects vector. Physiol. Mol. Plant Pathol. 67:212-219. doi:10.1016/j.pmpp.2006.02.001.
Schneider, B., K.S. Gibb, and E. Seemüller. 1997. Sequences and RFLP analysis of the elongation factor Tu gene used in differentiation and classification of phytoplasmas. Microbiology 143:3381-3389. doi:10.1099/00221287-143-10-3381.
Schneider, B., E. Seemüller, C.D. Smart, and B.C. Kirkpatrick. 1995. Phylogenetic classification of plant pathogenic mycoplasma-like organisms or phytoplasmas. In: S. Razin, and J.G. Tully, editors, Molecular microbial and diagnostic procedures in mycoplasmology. Academic press, CA, USA. p. 369-380.
Seemüller, E., M. Garnier, and B. Schneider. 2002. Mycoplasmas of plants and insects. In: S. Razin, and R. Herrmann, editors, Molecular biology and pathogenicity of mycoplasmas. Springer, Boston, MA, USA. p. 91-115.
Seemüller, E., and B. Schneider. 2007. Differences in virulence and genomic features of strains of ‘Candidatus phytoplasma mali’, the apple proliferation agent. Phytopathology 97:964-970. doi:10.1094/PHYTO-97-8-0964.
Smart, C.D., B. Schneider, C.L. Blomquist, L.J. Guerra, N.A. Harrison, U. Ahrens, K.H. Lorenz, E. Seemüller, and B.C. Kirkpatrick. 1996. Phytoplasma-specific PCR primers based on sequences of the 16S-23S rRNA spacer region. Appl. Environ. Microbiol. 62:2988-2993.
Sugawara, K., M. Himeno, T. Keima, Y. Kitazawa, K. Maejima, K. Oshima, and S. Namba. 2012. Rapid and reliable detection of phytoplasma by loop-mediated isothermal amplification targeting a housekeeping gene. J. Gen. Plant Pathol. 78:389-397. doi:10.1007/s10327-012-0403-9.
Tan, M.C., H.C. Li, W.N. Tsao, W.L. Su, T.Y. Lu, H.S. Chang, Y.Y. Lin, C.J. Liou, C.L. Hsish, Z.J. Yu, R.C. Sheue, Y.S. Wang, F.C. Lee, and Y.J. Yang. 2016. Phytoplasma SAP11 alters 3-isobutyl-2-methoxypyrazine biosynthesis in Nicotina benthamiana by suppressing NbOMT1. J. Exp. Bot. 67:1-11. doi:10.1093/jxb/erw225.
The IRPCM Phytoplasma/Spiroplasma Working Team-Phytoplasma Taxonomy Group. 2004. ‘Candidatus Phytoplasma’, a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. Int. J. Syst. Evol. Microbiol. 54:1243-1255. doi:10.1099/ijs.0.02854-0.
Tomlinson, J., N. Boonham, and M. Dickinson. 2010. Development and evaluation of a one-hour DNA extraction and loop-mediated isothermal amplification assay for rapid detection of phytoplasmas. Plant Pathol. 59:465-471. doi:10.1111/j.1365-3059.2009.02233.x.
Torres, E., E. Bertolini, M. Cambra, C. Montón, and P.M. Martín. 2005. Real-time PCR for simultaneous and quantitative detection of quarantine phytoplasmas from apple proliferation (16SrX) group. Mol. Cell. Probes. 19:334-340. doi:10.1016/j.mcp.2005.06.002.
Tran-Nguyen, L.T.T., M. Kube, B. Schneider, R. Reinhardt, and K.S. Gibb. 2008. Comparative genome analysis of “Candidatus Phytoplasma australiense” (Subgroup tuf-Australia I; rp-A) and “Ca. Phytoplasma asteris” strains OY-M and AY-WB. J. Bacteriol. 190:3979-3991. doi:10.1128/JB.01301-07.
Wei, W., E.R. Davis, M.I. Lee, and Y. Zhao. 2007. Computer-simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. Int. J. Syst. Evol. Microbiol. 57:1855-1867. doi:10.1099/ijs.0.65000-0.
Wei, W., S. Kakizawa, S. Suzuki, H.Y. Jung, H. Nishigawa, S.I. Miyata, K. Oshima, M. Ugaki, T. Hibi, and S. Namba. 2004. In planta dynamic analysis of onion yellows phytoplasma using localized inoculation by insect transmission. Phytopathology 94:244-250. doi:10.1094/PHYTO.2004.94.3.244.
Yasuhara-Bell, J., F. Baysal-Gurel, S.A. Miller, and A.M. Alvarez. 2015. Utility of a loopmediated amplification assay for detection of Clavibacter michiganensis subsp. michiganensis in seeds and plant tissues. Can. J. Plant Pathol. 37:260-266. doi:10.1080/07060661.2015.1053988.
Zamorano, A., and N. Fiore. 2016. Draft genome of 16SrIII-J phytoplasma, a plant pathogenic bacterium with a broad spectrum of hots. Genome Announc. 4(3):e00602-16. doi:10.1128/genomeA.00602-16.
Zhao, Y., W. Wei, I.M. Lee, J. Shao, X. Sou, and R.E. Davis. 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. doi:10.1099/ijs.0.010249-0.
Zhu, Y., Y. He, Z. Zheng, J. Chen, Z. Wang, and G. Zhou. 2017. Draft genome sequence of Rice Orange Leaf Phytoplasma from Guangdong, China. Genome Announc. 5(22)e00430-17. doi:10.1128/genomeA.00430-17.
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