The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Trunk Injection of Citrus Trees with a Polymeric Nanobactericide Reduces Huanglongbing Severity Caused by Candidatus Liberibacter asiaticus

  • Received : 2023.12.05
  • Accepted : 2024.02.18
  • Published : 2024.04.01
Download PDF
⟨ Previous Next ⟩

Abstract

Huanglongbing (HLB) is a disease caused by the phloem-limited Candidatus Liberibacter asiaticus (CLas) that affects the citrus industry worldwide. To date, only indirect strategies have been implemented to eradicate HLB. Included among these is the population control of the psyllid vector (Diaphorina citri), which usually provides inconsistent results. Even though strategies for direct CLas suppression seem a priori more promising, only a handful of reports have been focused on a confrontation of the pathogen. Recent developments in polymer chemistry have allowed the design of polycationic self-assembled block copolymers with outstanding antibacterial capabilities. Here, we report the use of polymeric nano-sized bactericide particles (PNB) to control CLas directly in the phloem vasculature. The field experiments were performed in Rioverde, San Luis Potosí, and is one of the most important citrusproducing regions in Mexico. An average 52% reduction in the bacterial population was produced when PNB was injected directly into the trunk of 20 infected trees, although, in some cases, reduction levels reached 97%. These results position PNB as a novel and promising nanotechnological tool for citrus crop protection against CLas and other related pathogens.

Keywords

Acknowledgement

The authors acknowledge the financial support provided by the Centro de Investigacion en Quimica Aplicada (CIQA), through grant N° 6495/6679/2022. This study was partially supported by the Program "Investigadoras e Investigadores por Mexico" from the Consejo Nacional de Humanidades, Ciencia y Tecnologia (CONAHCyT) (Project No. 1333 to JHVS). The authors also acknowledge Iliana Marcela Rodriguez Salinas for her valuable technical support during earlier experiments with PNB.

References

  1. Alquezar, B., Carmona, L., Bennici, S., Miranda, M. P., Bassanezi, R. B. and Pena, L. 2022. Cultural management of huanglongbing: current status and ongoing research. Phytopathology 112:11-25. https://doi.org/10.1094/PHYTO-08-21-0358-IA
  2. Archer, L., Albrecht, U. and Crane, J. 2021. Trunk injection to deliver crop protection materials: an overview of basic principles and practical considerations. IFAS Extension No. HS1426. Institute of Food and Agricultural Sciences (IFAS), Gainesville, FL, USA. 9 pp.
  3. Archer, L., Kunwar, S., Alferez, F., Batuman, O. and Albrecht, U. 2023. Trunk injection of oxytetracycline for huanglongbing management in mature grapefruit and sweet orange trees. Phytopathology 113:1010-1021. https://doi.org/10.1094/PHYTO-09-22-0330-R
  4. Bassanezi, R. B., Montesino, L. H., Gasparoto, M. C. G., Bergamin-Filho, A. and Amorim, L. 2011. Yield loss caused by Huanglongbing in different sweet orange cultivars in Sao Paulo, Brazil. Eur. J. Plant Pathol. 130:577-586. https://doi.org/10.1007/s10658-011-9779-1
  5. Bassanezi, R. B., Montesino, L. H. and Stuchi, E. S. 2009. Effects of huanglongbing on fruit quality of sweet orange cultivars in Brazil. Eur. J. Plant Pathol. 125:565-572. https://doi.org/10.1007/s10658-009-9506-3
  6. Blaustein, R. A., Lorca, G. L. and Teplitski, M. 2018. Challenges for managing Candidatus Liberibacter spp. (huanglongbing disease pathogen): current control measures and future directions. Phytopathology 108:424-435.
  7. Bove, J. M. 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 88:7-37.
  8. Bove, J. M. and Ayres, A. J. 2007. Etiology of three recent diseases of citrus in Sao Paulo State: sudden death, variegated chlorosis and huanglongbing. IUBMB Life 59:346-354. https://doi.org/10.1080/15216540701299326
  9. Croxton, S. D. and Stansly, P. A. 2014. Metalized polyethylene mulch to repel Asian citrus psyllid, slow spread of huanglongbing and improve growth of new citrus plantings. Pest Manag. Sci. 70:318-323. https://doi.org/10.1002/ps.3566
  10. da Graca, J. V. and Korsten, L. 2004. Citrus huanglongbing: review, present status, and future strategies. In: Disease of fruits and vegetables, ed. by S. A. M. H. Naqci, Vol. 1, pp. 229-245. Springer, Dordrecht, the Netherlands.
  11. do Carmo Teixeira, D., Saillard, C., Eveillard, S., Danet, J. L., da Costa, P. I., Ayres, A. J. and Bove, J. 2005. 'Candidatus Liberibacter americanus', associated with citrus huanglongbing (green disease) in Sao Paulo State, Brazil. Int. J. Syst. Evol. Microbiol. 55:1857-1862. https://doi.org/10.1099/ijs.0.63677-0
  12. Folimonova, S. Y., Robertson, C. J., Garnsey, S. M., Gowda, S. and Dawson, W. O. 2009. Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology 99:1346-1354. https://doi.org/10.1094/PHYTO-99-12-1346
  13. Flores-Sanchez, J. L., Mora-Aguilera, G., Loeza-Kuk, E., LopezArroyo, J. I., Dominguez-Monge, S., Acevedo-Sanchez, G. and Robles-Garcia, P. 2015. Yield loss caused by Candidatus Liberibacter asiaticus in Persian lime, in Yucatan Mexico. Rev. Mex. Fitopatol. 33:195-210.
  14. Gaire, S., Albrecht, U., Batuman, O., Qureshi, J., Zekri, M. and Alferez, F. 2022. Individual protective covers (IPCs) to prevent Asian citrus psyllid and Candidatus Liberibacter asiaticus from establishing in newly planted citrus trees. Crop Prot. 152:105862.
  15. Garcia-Sanchez, A. N., Yanez-Macias, R., Hernandez-Flores, J. L., Alvarez-Morales, A., Valenzuela-Soto, J. H., GuerreroSanchez, C. and Guerrero-Santos, R. 2021. Exogenous application of polycationic nanobactericide on tomato plants reduces the Candidatus Liberibacter solanacearum infection. Plants 10:2096.
  16. Gottwald, T. R., Graham, J. H., Irey, M. S., McGollum, T. G. and Wood, B. W. 2012. Inconsequential effect of nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress. Crop Prot. 36:73-82. https://doi.org/10.1016/j.cropro.2012.01.004
  17. Hung, T.-H., Hung, S.-C., Chen, C.-N., Hsu, M.-H. and Su, H.-J. 2004. Detection by PCR of Candidatus Liberibacter asiaticus, the bacterium causing citrus huanglongbing in vector psyllids: application to the study of vector-pathogen relationships. Plant Pathol. 53:96-102. https://doi.org/10.1111/j.1365-3059.2004.00948.x
  18. Jagoueix, S., Bove, J. M. and Garnier, M. 1994. The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. Int. J. Bacteriol. 44:379-386. https://doi.org/10.1099/00207713-44-3-379
  19. Jagoueix, S., Bove, J. M. and Garnier, M. 1996. PCR detection of the two 'Candidatus' Liberobacter species associated with greening disease of citrus. Mol. Cell Probes 10:43-50. https://doi.org/10.1006/mcpr.1996.0006
  20. Koh, E.-J., Zhou, L., Williams, D. S., Park, J., Ding, N., Duan, Y.-P. and Kang, B.-H. 2012. Callose deposition in the phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with "Candidatus Liberibacter asiaticus". Protoplasma 249:687-697. https://doi.org/10.1007/s00709-011-0312-3
  21. Li, J., Kolbasov, V. G., Lee, D., Pang, Z., Huang, Y., Collins, N. and Wang, N. 2020. Residue dynamics of streptomycin in citrus delivered by foliar spray and trunk injection and effect on 'Candidatus Liberibacter asiaticus' titer. Phytopathology 111:1095-1103. https://doi.org/10.1094/PHYTO-09-20-0427-R
  22. Li, J., Kolbasov, V. G., Pang, Z., Duan, S., Lee, D., Huang, Y., Xu, J., Teper, D., Lamichhane, T. and Wang, N. 2021. Evaluation of the control effect of SAR inducers against citrus Huanglongbing applied by foliar spray, soil drench or trunk injection. Phytopathol. Res. 3:2
  23. Li, J., Trivedi, P. and Wang, N. 2016. Field evaluation of plant defense inducers for the control of citrus huanglongbing. Phytopathology 106:37-46. https://doi.org/10.1094/PHYTO-08-15-0196-R
  24. Li, W., Hartung, J. S. and 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
  25. Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  26. Lopes, S. A., Bertolini, E., Frare, G. F., Martins, E. C., Wulff, N. A., Teixeira, D. C., Fernandes, N. G. and Cambra, M. 2009. Graft transmission efficiencies and multiplication of 'Candidatus Liberibacter americanus' and 'Ca. Liberibacter asiaticus' in citrus plants. Phytopathology 99:301-306.
  27. Mora-Aguilera, G., Robles-Garcia, P., Lopez-Arroyo, J. I., FloresSanchez, J., Acevedo-Sanchez, G., Dominguez-Monge, S., Gutierrez-Sepinisa, A. and Loeza-Kuk, E. 2014. Current situation and prospects for management of citrus HLB. Rev. Mex. Fitopatol. 32:108-119.
  28. Orce, I. G., Sendin, L. N., Marano, M. R., Vojnov, A. A., Castagnaro, A. P. and Filippone, M. P. 2014. Novel set of realtime PCR primers for simultaneous detection of Liberibacter species associated with citrus huanglongbing. Sci. Agric. 72:252-259. https://doi.org/10.1590/0103-9016-2013-0417
  29. Servicio de Informacion Agroalimentaria y Pesquera (SIAP). 2022. Anuario estadistico de la produccion agricola. Gobierno de Mexico. URL https://nube.siap.gob.mx/cierreagricola/ [15 January 2023].
  30. Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria (SENASICA). 2023. Agriculture launches comprehensive agronomic plan to protect national citrus production. Gobierno de Mexico. URL https://www.gob.mx/senasica/documentos/agriculture-launches-comprehensive-agronomic-plan-to-protect-national-citrus-production [15 January 2023].
  31. Stansly, P. A., Arevalo, H. A., Qureshi, J. A., Jones, M. M., Hendricks, K., Roberts, P. D. and Roka, F. M. 2014. Vector control and foliar nutrition to maintain economic sustainability of bearing citrus in Florida groves affected by huanglongbing. Pest Manage. Sci. 70:415-426. https://doi.org/10.1002/ps.3577
  32. Stephano-Hornedo, J. L., Torres-Gutierrez, O., Toledano-Magana, Y., Gradilla-Martinez, I., Prestyakov, A., Sanchez-Gonzalez, A., Garcia-Ramos, J. C. and Bogdanchikova, N. 2020. ArgovitTM silver nanoparticles to fight huanglongbing disease in Mexican limes (Citrus aurantifolia Swingle). RSC Adv. 10:6146-6155. https://doi.org/10.1039/C9RA09018E
  33. Trinidad-Cruz, J. R., Rincon-Enriquez, G., Quinones-Aguilar, E. E., Arce-Leal, A. P. and Leyva-Lopez, N. E. 2019. Inductors of plant resistance in the control of Candidatus Liberibacter asiaticus in Mexican lemon (Citrus aurantifolia) trees. Rev. Mex. Fitopatol. 37:304-317.
  34. Wang, N., Pierson, E. A., Setubal, J. C., Xu, J., Levy, J. G., Zhang, Y., Li, J., Rangel, L. T. and Martins, J. Jr. 2017. The Candidatus Liberibacter-host interface: insights into pathogenesis mechanisms and disease control. Annu. Rev. Phytopathol. 55:451-482. https://doi.org/10.1146/annurev-phyto-080516-035513
  35. Wise, J. C., VanWoerkom, A. H., Acimovic, S. G., Sundin, G. W., Cregg, B. M. and Vandervoort, C. 2014. Trunk injection: a discriminating delivering system for horticulture crop IPM. Entomol. Ornithol. Herpetol. 3:100126.
  36. Yanez-Macias, R., Alvarez-Moises, I., Perevyazko, I., Lezov, A., Guerrero-Santos, R., Schubert, U. S. and Guerrero-Sanchez, C. 2017. Effect of the degree of quaternization and molar mass on the cloud point of poly[2-(dimethylamino)ethyl methacrylate] aqueous solutions: a systematic investigation. Macromol. Chem. Phys. 218:1700065.
  37. Zhang, M., Powell, C. A., Guo, Y., Benyon, L. and Duan, Y. 2013. Characterization of the microbial community structure of Candidatus Liberibacter asiaticus-infected citrus plants treated with antibiotics in the field. BMC Microbiol. 13:112.
  38. Zhang, M., Powell, C. A., Zhou, L., He, Z., Stover, E. and Duan, Y. 2011. Chemical compounds effective against citrus huanglongbing bacterium 'Candidatus Liberibacter asiaticus' in planta. Phytopathology 101:1097-1103. https://doi.org/10.1094/PHYTO-09-10-0262