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Conventional and qPCR reveals the presence of ‘Candidatus Liberibacter solanacearum’ haplotypes A, and B in Physalis philadelphica plant, seed, and Βactericera cockerelli psyllids, with the assignment of a new haplotype H in Convolvulaceae

  • Alejandra Contreras-Rendón
  • Jesús Ricardo Sánchez-Pale
  • Dionicio Fuentes-Aragón
  • Iobana Alanís-Martínez
  • Hilda Victoria Silva-RojasEmail author
Original Paper
  • 70 Downloads

Abstract

The husk tomato (Physalis philadelphica Lam.) is an important Solanaceae native to Mesoamerica that is grown for its green fruit used as an important ingredient in domestic and international cuisine. Nevertheless, husk tomato plants with symptoms resembling those caused by ‘Candidatus Liberibacter solanacearum’ (CLso) have been observed during the last decade in plantations located in the State of Mexico, Michoacan and Sinaloa in Mexico. These areas are located near other solanaceous crops where Bactericera cockerelli the well-known psyllid transmitter of CLso is frequently present. Thus, the goal of this study was to determine if CLso haplotypes are present in husk tomato varieties in commercial fields in Mexico. From 2015 to 2016, plants and fruit showing evident symptoms of CLso infection, as well as psyllids were collected in these states and assayed by PCR for CLso using primer sets OA2/OI2c and LpFrag 1-25F/427R. Phylogenetic reconstruction was performed with Bayesian analysis and maximum likelihood methods using amplicon sequences obtained in this work along with those deposited in the GenBank database corresponding to the CLso detected in Solanaceae, Apiaceae, and Convolvulaceae host families. In addition, all the sequences were subjected to haplotype determination through an analysis of DNA polymorphisms using the DnaSP software. Furthermore, quantitative PCR (qPCR) was performed using CLso-specific primers and probes. Phylogenetic reconstruction and qPCR confirmed the presence of CLso in plants, seeds and insect-vectors, and CLso sequences from plants and seeds completely matched haplotype B, whereas CLso haplotypes A and B were detected in B. cockerelli psyllids. Polymorphism analysis identified a novel Convolvulaceae-associated CLso haplotype, which was named haplotype H. The results of this study will enable the dissemination of infected seeds to new husk tomato production areas to be avoided.

Keywords

CLso detection Husk tomato Identification Molecular phylogeny Seed 

Notes

Acknowledgements

The authors thank the Universidad Autonoma del Estado de Mexico, to the Laboratory of Seed Biotechnology and Plant Pathology at the Postgraduate College at Montecillo Campus through project (Grant No. CM 17-4011) for financial support of the present study and for allowing us the use of the sequencing facility unit.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Aguilar E, Sengoda VG, Bextine B, McCue KF, Munyaneza JE (2013a) First report of ‘Candidatus Liberibacter solanacearum’ on tomato in Honduras. Plant Dis 97:1375.  https://doi.org/10.1094/PDIS-04-13-0354-PDN CrossRefPubMedGoogle Scholar
  2. Aguilar E, Sengoda VG, Bextine B, McCue KF, Munyaneza JE (2013b) First report of ‘Candidatus Liberibacter solanacearum’ on tobacco in Honduras. Plant Dis 97:1376.  https://doi.org/10.1094/PDIS-04-13-0453-PDN CrossRefPubMedGoogle Scholar
  3. Alfaro-Fernández A, Siverio F, Cebrián C, Villaescusa FJ, Font MI (2012a) ‘Candidatus Liberibacter solanacearum’ associated with Bactericera trigonica affected carrots in the Canary Islands. Plant Dis 96:581.  https://doi.org/10.1094/PDIS-10-11-0878-PDN CrossRefPubMedGoogle Scholar
  4. Alfaro-Fernández A, Cebrián C, Villaescusa FJ, Hermoso de Mendoza A, Ferrándiz JC, SanJuán S, Font MI (2012b) First report of ‘Candidatus Liberibacter solanacearum’ in carrot in mainland Spain. Plant Dis 96:582.  https://doi.org/10.1094/PDIS-11-11-0918-PDN CrossRefPubMedGoogle Scholar
  5. Alfaro-Fernández A, Hernández-Llopis D, Font MI (2017) Haplotypes of ‘Candidatus Liberibacter solanacearum’ identified in Umbeliferous crops in Spain. Eur J Plant Pathol 149:127–131.  https://doi.org/10.1007/s10658-017-1172-2 CrossRefGoogle Scholar
  6. Antolinez CA, Fereres A, Moreno A (2017) Risk assessment of ‘Candidatus Liberibacter solanacearum’ transmission by the psyllids Bactericera trigonica and B tremblayi from Apiaceae crops to potato. Sci Re 7:45534.  https://doi.org/10.1038/srep45534 CrossRefGoogle Scholar
  7. Bertolini E, Teresani GR, Loiseau M, Tanaka FAO, Barbe S, Martinez C (2015) Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathol 64:276–285.  https://doi.org/10.1111/ppa.12245 CrossRefGoogle Scholar
  8. Bextine B, Arp A, Flores E, Aguilar E, Lastrea L, Soza-Gomez F, Poweall C, Rueda A (2013a) First report of zebra chip and ‘Candidatus Liberibacter solanacearum’ on potatoes in Nicaragua. Plant Dis 97:1109.  https://doi.org/10.1094/PDIS-09-12-0824-PDN CrossRefPubMedGoogle Scholar
  9. Bextine B, Aguilar E, Rueda A, Caceres O, Sengoda VG, McCue KF, Munyaneza JE (2013b) First report of ‘Candidatus Liberibacter solanacearum’ on tomato in El Salvador. Plant Dis 97:1245.  https://doi.org/10.1094/PDIS-03-13-0248-PDN CrossRefPubMedGoogle Scholar
  10. Butler CD, Trumble JT (2012) The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terr Arthropod Rev 5:87–111.  https://doi.org/10.1163/187498312X634266 CrossRefGoogle Scholar
  11. CABI (2017) Centre for Agricultural Bioscience International. Invasive species compendium, ‘Candidatus Liberibacter solanacearum’ datasheet. https://www.cabi.org/isc/datasheet/109434. Accessed on 9 Dec 2018
  12. Camacho-Tapia M, Rojas-Martinez RI, Zavaleta-Mejia E, Hernandez-Deheza MG, Carrillo-Salazar JA, Rebollar-Alviter A, Ochoa-Martinez DL (2011) Aetiology of chili pepper variegation from Yurecuaro, Mexico. J Plant Pathol 93:331–335.  https://doi.org/10.4454/jpp.v93i2.1187 CrossRefGoogle Scholar
  13. Contreras-Rendon A, Gutierrez-Ibañez AT, Silva-Rojas HV, Sanchez-Pale JR, Laguna-Cerda A, Ramirez-Davila JF (2016) Spatial distribution of ‘Candidatus Liberibacter solanacearum’ and Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) in potato (Solanum tuberosum L.). Southwest Entomol 41:105–114.  https://doi.org/10.3958/059.041.0112 CrossRefGoogle Scholar
  14. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nat Methods 9:772.  https://doi.org/10.1038/nmeth.2109 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  16. French-Monar RD, Patton AFIII, Douglas JM, Abad JA, Schuster G, Wallace RW, Wheeler TA (2010) First report of ‘Candidatus Liberibacter solanacearum’ on field tomatoes in the United States. Plant Dis 94:481.  https://doi.org/10.1094/PDIS-94-4-0481A CrossRefPubMedGoogle Scholar
  17. González-Mendoza D, Ascencio-Martinez D, Hau Poox A, Mendez-Trujillo V, Grimaldo-Juarez O, Santiaguillo Hernández JF, Cervantes-Diaz L, Aviles-Marin SM (2011) Phenolic compounds and physiochemical analysis of Physalis ixocarpa genotypes. Sci Res Essays 6:3808–3814.  https://doi.org/10.5897/SRE11.570 CrossRefGoogle Scholar
  18. Haapalainen M (2014) Biology and epidemics of ‘Candidatus Liberibacter’ species, psyllid-transmitted plant pathogenic bacteria. Ann Appl Biol 165:172–198.  https://doi.org/10.1111/aab.12149 CrossRefGoogle Scholar
  19. Haapalainen M, Wang J, Latvala S, Lehtonen MT, Pirhonen M, Nissinen AI (2018) Genetic variation of ‘Candidatus Liberibacter solanacearum’ haplotype C and identification of a novel haplotype from Trioza urticae and stinging nettle. Phytopathology 108:925–934.  https://doi.org/10.1094/PHYTO-12-17-0410-R CrossRefPubMedGoogle Scholar
  20. Hajri A, Loiseau M, Cousseau-Suhard P, Renaudin I, Gentit P (2017) Genetic characterization of ‘Candidatus Liberibacter solanacearum’ haplotypes associated with apiaceous crops in France. Plant Dis 101:1383–1390.  https://doi.org/10.1094/PDIS-11-16-1686-RE CrossRefPubMedGoogle Scholar
  21. Hajri A, Cousseau-Suhard P, Gentit P, Loiseau M (2019) New insights into the genetic diversity of the bacterial plant pathogen ‘Candidatus Liberibacter solanacearum’ as revealed by a new multilocus sequence analysis scheme. CSH Protoc.  https://doi.org/10.1101/623405 CrossRefGoogle Scholar
  22. Hansen AK, Trumble JT, Stouthamer R, Paine TD (2008) A new huanglongbing species ‘Candidatus Liberibacter psyllaurous’ found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Appl Environ Microbiol 74:5862–5865.  https://doi.org/10.1128/AEM.01268-08 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Harlan JR (1971) Agricultural origins: centers and noncenters. Science 174:468–474CrossRefGoogle Scholar
  24. Jagoueix S, Bove JM, Garnier M (1994) The phoem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. Int J Syst Bacteriol 44:379–386.  https://doi.org/10.1099/00207713-44-3-379 CrossRefPubMedGoogle Scholar
  25. Leigh JW, Bryant D (2015) PopART: Full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116.  https://doi.org/10.1111/2041-210X.12410 CrossRefGoogle Scholar
  26. Levy J, Ravindran A, Gross D, Tamborindeguy C, Pierson E (2011) Translocation of ‘Candidatus Liberibacter solanacearum’, the zebra chip pathogen, in potato and tomato. Phytopathology 101:1285–1291.  https://doi.org/10.1094/PHYTO-04-11-0121 CrossRefPubMedGoogle Scholar
  27. Li W, Hartung JS, Levy L (2006) Quantitative real-time PCR for detection and identification of ‘Candidatus Liberibacter’ species associated with citrus huanglongbing. J Microbiol Methods 66:104–115.  https://doi.org/10.1016/j.mimet.2005.10.018 CrossRefGoogle Scholar
  28. Li W, Abad JA, French-Monar RD, Rascoe J, Wen A, Gudmestad NC, Secor GA, Ing-Ming L, Duan Y, Levy L (2009) Multiplex real-time PCR for detection, identification and quantification of ‘Candidatus Liberibacter solanacearum’ in potato plants with zebra chip. J Microbiol Methods 78:53–65.  https://doi.org/10.1016/j.mimet.2009.04.009 CrossRefGoogle Scholar
  29. Liefting LW, Perez-Egusquiza ZC, Clover GRG, Anderson JAD (2008a) A new ‘Candidatus Liberibacter’ species in Solanum tuberosum in New Zealand. Plant Dis 92:1474.  https://doi.org/10.1094/PDIS-92-10-1474A CrossRefPubMedGoogle Scholar
  30. Liefting LW, Ward LI, Shiller JB, Clover GRG (2008b) A new ‘Candidatus Liberibacter’ species in Solanum betaceum (tamarillo) and Physalis peruviana (Cape gooseberry) in New Zealand. Plant Dis 92:1588.  https://doi.org/10.1094/PDIS-92-11-1588B CrossRefPubMedGoogle Scholar
  31. Liefting LW, Weir BS, Pennycook SR, Clover GRG (2009) ‘Candidatus Liberibacter solanacearum’ associated with plants in the family Solanaceae. Int J Syst Evol Microbiol 59:2274–2276.  https://doi.org/10.1099/ijs.0.007377-0 CrossRefPubMedGoogle Scholar
  32. Ling KS, Lin H, Lewis-Ivey ML, Zhang W, Miller SA (2011) First report of ‘Candidatus Liberibacter solanacearum’ naturally infecting tomatoes in the State of Mexico, Mexico. Plant Dis 95:1026.  https://doi.org/10.1094/PDIS-05-11-0365 CrossRefPubMedGoogle Scholar
  33. Loiseau M, Gamier S, Boirin V, Merieau M, Leguay A, Renaudin I, Renvoise P, Gentit P (2014) First report of ‘Candidatus Liberibacter solanacearum’ on carrot in France. Plant Dis 98:839.  https://doi.org/10.1094/PDIS-08-13-0900-PDN CrossRefPubMedGoogle Scholar
  34. Mauck KE, Sun P, Meduri V, Hansen AK (2019) New Ca. Liberibacter psyllaurous haplotype resurrected from a 49-year-old specimen of Solanum umbelliferum: a native host of the psyllid vector. Sci Rep 9(9530):1–3.  https://doi.org/10.1038/s41598-019-45975-6 CrossRefGoogle Scholar
  35. Mawassi M, Dror O, Bar-Joseph M, Piasezky A, Sjölund JM, Levitzky N, Shoshana N, Meslenin L, Haviv S, Porat C, Katsir L, Kontsedalov S, Ghanim M, Zelinger-Reichert E, Arnsdorf YM, Gera A, Bahar O (2018) ‘Candidatus Liberibacter solanacearum’ is tightly associated with carrot yellows symptoms in Israel and transmitted by the prevalent psyllid vector Bactericera trigonica. Phytopathology 108:1056–1066.  https://doi.org/10.1094/PHYTO-10-17-0348-R CrossRefPubMedGoogle Scholar
  36. Mendoza-Herrera A, Levy J, Harrison K, Yao J, Ibanez F, Tamborindeguy C (2018) Infection by ‘Candidatus Liberibacter solanacearum’ haplotypes A and B in Solanum lycopersicum ‘Moneymaker’. Plant Dis 102:2009–2015.  https://doi.org/10.1094/PDIS-12-17-1982-RE CrossRefPubMedGoogle Scholar
  37. Monger WA, Jeffries CJ (2016) First report of ‘Candidatus Liberibacter solanacearum’ in parsley (Petroselinum crispum) seed. New Dis Rep 34:31.  https://doi.org/10.5197/j.2044-0588.2016.034.031 CrossRefGoogle Scholar
  38. Monger WA, Jeffries CJ (2018) A survey of ‘Candidatus Liberibacter solanacearum’ in historical seed from collections of carrot and related Apiaceae species. Eur J Plant Pathol 150:803–815.  https://doi.org/10.1007/s10658-017-1322-6 CrossRefGoogle Scholar
  39. Morris J, Shiller J, Mann R, Smith G, Yen A, Rodoni B (2017) Novel ‘Candidatus Liberibacter’ species identified in the Australian eggplant psyllid, Acizzia solanicola. Microb Biotechnol 10:833–844.  https://doi.org/10.1111/1751-7915.12707 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Munyaneza JE (2012) Zebra chip disease of potato: Biology, epidemiology, and management. Am J Pot Res 89:329–350.  https://doi.org/10.1007/s12230-012-9262-3 CrossRefGoogle Scholar
  41. Munyaneza JE, Sengoda VG, Crosslin JM, de la Rosa-Lozano G, Sanchez A (2009a) First report of ‘Candidatus Liberibacter psyllaurous’ in potato tubers with zebra chip disease in Mexico. Plant Dis 93:552.  https://doi.org/10.1094/PDIS-93-5-0552A CrossRefPubMedGoogle Scholar
  42. Munyaneza JE, Sengoda VG, Crosslin JM, Garzon-Tiznado JA, Cardenas-Valenzuela OG (2009b) First report of ‘Candidatus Liberibacter solanacearum’ in pepper plants in Mexico. Plant Dis 93:1076.  https://doi.org/10.1094/PDIS-93-10-1076B CrossRefPubMedGoogle Scholar
  43. Munyaneza JE, Fisher TW, Sengoda VG, Garczynski SF, Nissinen A, Lemmetty A (2010) Association of ‘Candidatus Liberibacter solanacearum’ with the psyllid Trioza apicalis (Hemiptera: Triozidae) in Europe. J Econ Entomol 103:1060–1070.  https://doi.org/10.1603/EC10027 CrossRefPubMedGoogle Scholar
  44. Munyaneza JE, Sengoda VG, Stegmark R, Arvidsson AK, Anderbrant O, Yuvaraj JK, Rämert B, Nissinen A (2012a) First report of ‘Candidatus Liberibacter solanacearum’ associated with psyllid-affected carrots in Sweden. Plant Dis 96:453.  https://doi.org/10.1094/PDIS-10-11-0871 CrossRefPubMedGoogle Scholar
  45. Munyaneza JE, Sengoda VG, Sundheim L, Meadow R (2012b) First report of ‘Candidatus Liberibacter solanacearum’ associated with psyllid-affected carrots in Norway. Plant Dis 96:454.  https://doi.org/10.1094/PDIS-10-11-0870 CrossRefPubMedGoogle Scholar
  46. Munyaneza JE, Sengoda VG, Aguilar E, Bextine BR, McCue KF (2013a) First report of ‘Candidatus Liberibacter solanacearum’ infecting eggplant in Honduras. Plant Dis 97:1654.  https://doi.org/10.1094/PDIS-06-13-0641-PDN CrossRefPubMedGoogle Scholar
  47. Munyaneza JE, Sengoda VG, Aguilar E, Bextine BR, McCue KF (2013b) First report of ‘Candidatus Liberibacter solanacearum’ associated with psyllid-affected tobacco in Nicaragua. Plant Dis 97:1244.  https://doi.org/10.1094/PDIS-03-13-0247-PDN CrossRefPubMedGoogle Scholar
  48. Munyaneza JE, Sengoda VG, Aguilar E, Bextine B, McCue KF (2014) First report of ‘Candidatus Liberibacter solanacearum’ on pepper in Honduras. Plant Dis 98:154.  https://doi.org/10.1094/PDIS-06-13-0598-PDN CrossRefPubMedGoogle Scholar
  49. Munyaneza JE, Swisher KD, Hommes M, Willhauck A, Buck H, Meadow R (2015) First report of ‘Candidatus Liberibacter solanacearum’ associated with psyllid-infested carrots in Germany. Plant Dis 99:1269.  https://doi.org/10.1094/PDIS-02-15-0206-PDN CrossRefGoogle Scholar
  50. Murphy AF, Cating RA, Goyer A, Hamm PB, Rondon SI (2014) First report of natural infection by ‘Candidatus Liberibacter solanacearum’ in bittersweet nightshade (Solanum dulcamara) in the Columbia Basin of Eastern Oregon. Plant Dis 98:1425.  https://doi.org/10.1094/PDIS-05-14-0497-PDN CrossRefPubMedGoogle Scholar
  51. Nelson WR, Fisher TW, Munyaneza JE (2011) Haplotypes of ‘Candidatus Liberibacter solanacearum’ suggest long-standing separation. Eur J Plant Pathol 130:5–12.  https://doi.org/10.1007/s10658-010-9737-3 CrossRefGoogle Scholar
  52. Nelson WR, Sengoda VG, Alfaro-Fernandez AO, Font MI, Crosslin JM, Munyaneza JE (2013) A new haplotype of ‘Candidatus Liberibacter solanacearum’ identified in the Mediterranean region. Eur J Plant Pathol 135:633–639.  https://doi.org/10.1007/s10658-012-0121-3 CrossRefGoogle Scholar
  53. Othmen SB, Morán FE, Navarro I, Barbé S, Martínez C, Marco-Noales E, Chermiti B, López MM (2018) ‘Candidatus Liberibacter solanacearum’ haplotypes D and E in carrot plants and seeds in Tunisia. J Plant Pathol 100:197–207.  https://doi.org/10.1007/s42161-018-0045-7 CrossRefGoogle Scholar
  54. Ozaslan C, Farooq S, Onen H, Bukun B, Ozcan S, Gunal H (2016) Invasion potential of two tropical Physalis species in arid and semi-arid climates: effect of water-salinity stress and soil types on growth and fecundity. PLoS ONE 11(10):e0164369.  https://doi.org/10.1371/journal.pone.0164369 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Pitman AR, Drayton GM, Kraberger SJ, Genet RA, Scott IA (2011) Tuber transmission of ‘Candidatus Liberibacter solanacearum’ and its association with zebra chip on potato in New Zealand. Eur J Plant Pathol 129:389–398.  https://doi.org/10.1007/s10658-010-9702-1 CrossRefGoogle Scholar
  56. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542.  https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rozas J, Ferrer-Mata A, Sánchez-Del Barrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302.  https://doi.org/10.1093/molbev/msx248 CrossRefPubMedGoogle Scholar
  58. Sengoda et al (2013) Sengoda VG, Buchman JL, Henne DC, Pappu HR, Munyaneza JE (2013) ‘Candidatus Liberibacter solanacearum’ titer over time in Bactericera cockerelli (Hemiptera: Triozidae) after acquisition from infected potato and tomato plants. J Econ Entomol 106:1964–1972.  https://doi.org/10.1371/journal.pone.0093475.g00 CrossRefPubMedGoogle Scholar
  59. SIAP (2018) Servicio de Información Agroalimentaria y Pesquera. https://www.gob.mx/siap/acciones-y-programas/produccion-agricola-33119. Accessed on 24 March 2018
  60. Silva-Rojas HV, Contreras-Rendon A, Sanchez-Pale JR (2016) ‘Candidatus Liberibacter solanacearum’ associated to Physalis philadelphica, a new solanaceous host. Phytopathology 106(S4):100.  https://doi.org/10.1094/PHYTO-106-12-S4.100 CrossRefGoogle Scholar
  61. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337.  https://doi.org/10.1007/s13127-011-056-0 CrossRefGoogle Scholar
  62. Swisher-Grimm KD, Garczynski SF (2019) Identification of a new haplotype of ‘Candidatus Liberibacter solanacearum’ in Solanum tuberosum. Plant Dis 103:468–4774.  https://doi.org/10.1094/PDIS-06-18-0937-RE CrossRefPubMedGoogle Scholar
  63. Swisher-Grimm KD, Mustafa T, Rodney-Cooper W, Munyaneza JE (2018) Role of ‘Candidatus Liberibacter solanacearum’ and Bactericera cockerelli haplotypes in zebra chip incidence and symptom severity. Am J Potato Res 95:709–719.  https://doi.org/10.1007/s12230-018-9678-5 CrossRefGoogle Scholar
  64. Tahzima R, Maes M, Achbani EH, Swisher KD, Munyaneza JE, De Jonghe K (2014) First report of ‘Candidatus Liberibacter solanacearum’ on carrot in Africa. Plant Dis 98:1426.  https://doi.org/10.1094/PDIS-05-14-0509-PDN CrossRefPubMedGoogle Scholar
  65. Teresani GR, Bertolini E, Alfaro-Fernandez A, Martinez C, Tanaka FAO, Kitajima EW, Roselio M, Sanjuan S, Fernandiz JC, Lopez MM (2014) Association of ‘Candidatus Liberibacter solanacearum’ with a vegetative disorder of celery in Spain and development of real-time PCR method for its detection. Phytopathology 104:804–811.  https://doi.org/10.1094/PHYTO-07-13-0182-R CrossRefPubMedGoogle Scholar
  66. Thompson SM, Johnson CP, Lu AY, Frampton RA, Sullivar KL, Fiers MWEJ, Crowhurst RN, Pitman AR, Scott IAW, Wen A, Gudmestad NC, Smith GR (2015) Genomes of ‘Candidatus Liberibacter solanacearum’ haplotype A from New Zealand and the United States suggest significant genome plasticity in the species. Phytopathology 105:863–871.  https://doi.org/10.1094/PHYTO-12-14-0363-FI CrossRefPubMedGoogle Scholar
  67. Thomas JE, Geering ADW, Maynard G (2018) Detection of ‘Candidatus Liberibacter solanacearum” in tomato on Norfolk Island, Australia. Australas Plant Dis Notes 13:7.  https://doi.org/10.1007/s13314-018-0289-2 CrossRefGoogle Scholar
  68. Torres GL, Cooper WR, Horton DR, Swisher KD, Garczynski SF, Munyaneza JE, Barcenas NM (2015) Horizontal transmission of ‘Candidatus Liberibacter solanacearum’ by Bactericera cockerelli (Hemiptera: Triozidae) on Convolvulus and Ipomoea (Solanales: Convolvulaceae). PLoS ONE 10:e0142734.  https://doi.org/10.1371/journal.pone.0142734 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wen A, Johnson C, Gudmestad NC (2013) Development of a PCR assay for the rapid detection and differentiation of ‘Candidatus Liberibacter solanacearum’ haplotypes and their spatiotemporal distribution in the United States. Am J Potato Res 90:229–236.  https://doi.org/10.1007/s12230-012-9293-9 CrossRefGoogle Scholar
  70. Wen A, Mallik I, Alvarado VY, Pasche JS, Wang X, Li W, Levy LE, Lin H, Scholthof H, Mirkov E, Rush CM, Gudmestad NC (2009) Detection, distribution, and genetic variability of ‘Candidatus Liberibacter’ species associated with zebra complex disease of potato in North America. Plant Dis 93:1102–1115.  https://doi.org/10.1094/PDIS-93-11-1102 CrossRefPubMedGoogle Scholar
  71. Wilf P, Carvalho MR, Gandolfo MA, Cúneo NR (2017) Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355:71–75.  https://doi.org/10.1126/science.aag2737 CrossRefPubMedGoogle Scholar
  72. Workneh F, Paetzold L, Silva A, Johnson C, Rashed A, Badillo-Vargas I, Gudmestad NC, Rush CM (2018) Assessments of temporal variations in haplotypes of ‘Candidatus Liberibacter solanacearum’ and its vector, the potato psyllid, in potato fields and native vegetation. Environ Entomol 47:1184–1193.  https://doi.org/10.1093/ee/nvy106 CrossRefPubMedGoogle Scholar
  73. Zhang CR, Khan W, Bakht J, Nair MG (2016) New antiinflammatory sucrose esters in the natural sticky coating of tomatillo (Physalis philadelphica), an important culinary fruit. Food Chem 196:726–732.  https://doi.org/10.1016/j.foodchem.2015.10.007 CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Facultad de Ciencias AgricolasUniversidad Autonoma del Estado de MexicoTolucaMexico
  2. 2.Posgrado en Fitopatologia, FitosanidadColegio de PostgraduadosTexcocoMexico
  3. 3.Estacion Nacional de Epidemiologia, Cuarentena y Saneamiento VegetalSENASICAQueretaroMexico
  4. 4.Produccion de SemillasColegio de PostgraduadosTexcocoMexico

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