Methods for detecting Huanglongbing in citrus
DOI:
https://doi.org/10.29312/remexca.v15i4.3300Keywords:
diagnosis, images, PCR, sampling, spectrometry, symptomsAbstract
In Mexico, citrus farming represents one of the most important economic activities for national fruit growing, with a production of 8.8 million tonnes and an economic spillover of more than 47 billion pesos per year. Nonetheless, production is affected by pests and diseases, with Huanglongbing (HLB), ‘yellow dragon’ or citrus greening, standing out as the most devastating disease worldwide, caused by a proteobacterium of the genus Candidatus Liberibacter (Ca. L.). Because there is no effective method to control this disease, correct and timely detection can significantly reduce its spread. The purpose of this review is to compile methods used for detecting the presence of Ca. L. in citrus plants, covering general aspects of the symptomatology of the disease, molecular methods for accurate and rapid detection when sampling both in plants and in the vector. In addition, different protocols are mentioned that analyze some compounds produced during infection with Ca. L. and images in citrus with HLB.
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Aksenov, A. A.; Pasamontes, A.; Peirano, D. J.; Zhao, W.; Dandekar, A. M.; Fiehn, O.; Ehsani, R. and Davis, C. E. 2014. Detection of huanglongbing disease using differential mobility spectrometry. Anal. Chem. 86(5):2481-2488. https://doi.org/10.1021/ac403469y.
Alanís-Martínez, E. I.; Rojas-Martínez, R. I. y Cora-Valencia, E. 2013. Detección del fitoplasma del grupo 16SrIX, estrechamente relacionado a pigeon pea witches´broomphytoplasm, en plantas de cítricos con síntomas asociados a HLB. Póster presentado al XL Congreso Nacional y XV Congreso Internacional de la Sociedad Mexicana de Fitopatología, Huatulco, México.
Arredondo-Valdés, R.; Delgado-Ortiz, J. C.; Beltrán-Beache, M.; Anguiano-Cabello, J.; Cerna-Chávez, E.; Rodríguez-Pagaza, Y. and Ochoa-Fuentes, Y. M. 2016. A review of techniques for detecting Huanglongbing (greening) in citrus. Can J. Microbiol. 62(10):803-811. https://doi.org/10.1139/cjm-2016-0022.
Bové, J. M. 2006. Huanglongbing: a destructive, newly emerging, century old disease of citrus. J. Plant Pathol. 88(1):7-37.
Bové, J. M. 2014. Huanglongbing or yellow shoot, a disease of gondwanan origin: will it destroy citrus worldwide? Phytoparasitica. 42(5):579-583. https://doi.org/10.1007/s12600-014-0415-4.
Chen, J.; Pu, X.; Deng, X.; Liu, S.; Li, H. and Civerolo, E. 2009. A phytoplasma related to ‘Candidatus Phytoplasma asteris’ detected in citrus showing huanglongbing (yellow shoot disease) symptoms in guangdong, PR China. Phytopathology. 99(3):236-242. https://doi.org/10.1094/phyto-99-3-0236.
Davis, M. J.; Mondal, S. N.; Chen, H.; Rogers, M. E. and Brlansky, R. H. 2008. Co-cultivation of ‘Candidatus Liberibacter asiaticus’ with actinobacteria from citrus with huanglongbing. Plant Dis. 92(11):1547-1550. https://doi.org/10.1094/pdis-92-11-1547.
Demeke, T. and Jenkins, G. R. 2010. Influence of DNA extraction methods, PCR inhibitors and quantification methods on real time PCR assay of biotechnology derived traits. Anal. Bioanal. Chem. 396(6):1977-1990. https://doi.org/10.1007/s00216-009-3150-9.
Deng, X.; Zhou, G.; Li, H.; Chen, J. and Civerolo, L. E. 2007. Nested PCR detection and sequence confirmation of ‘Candidatus Liberibacter asiaticus’ from Murraya paniculata in guangdong, China. Dis. Notes. 91(8):1051. https://doi.org/10.1094/PDIS-91-8-1051C.
Ding, F.; Yi, G. and Wang, G. 2004. Research on the PCR and nested PCR detection of citrus huanglongbing. Acta Hortic. Sin. 31(6):803-806. https://www.ahs.ac.cn/EN/Y2004/V31/I6/803.
Ding, F.; Paul, C.; Brlansky, R. and Hartung, J. S. 2017. Immune tissue print and immunecapture PCR for diagnosis and detection of Candidatus Liberibacter asiaticus. Sci. Rep. 7(1):46467. https://doi.org/10.1038/srep46467.
Doyle, J. J. and Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19(1):11-15.
EPPO. 2014. European and mediterranean plant protection organization. Liberibacter americanus’ and ‘Candidatus Liberibacter asiaticus’. EPPO Bull. 44(1):376-389. https://doi.org/10.1111/epp.12161.
Fujikawa, T. and Iwanami, T. 2012. Sensitive and robust detection of citrus Greening (Huanglongbing) bacterium “Candidatus Liberibacter asiaticus” by DNA amplification with new 16S rdna-specific primers. Mol. Cell. Probes. 26(5):194-197. https://doi.org/10.1016/j.mcp.2012.06.001.
Fujikawa, K.; Iwanami, T. and Fujikawa, T. 2018. Alterations of Candidatus Liberibacter asiaticus associated microbiota decrease survival of Ca. L. asiaticus in in vitro assays. Front. Microbiol. 9(1):3089. https://doi.org/10.3389/fmicb.2018.03089.
Garcia-Ruiz, F.; Sankaran, S.; Maja, J. M.; Lee, W. S.; Rasmussen, J. and Ehsani, R. 2013. Comparison of two aerial imaging platforms for identification of huanglongbing infected citrus trees. Comput. Electron. Agric. 91(2):106-115.
Garnier, M. and Bové, J. M. 1993. Citrus greening disease. In: proceedings of the twelfth conference of the international organization of citrus virologists IOCV. american phytopathological press. Riverside, CA. 212-219 pp.
Gómez-Flores, W.; Garza-Saldaña, J. J. and Varela-Fuentes, S. E. 2019. Detection of Huanglongbing disease based on intensity-invariant texture analysis of images in the visible spectrum. Comput. Electron. Agric. 162(7):825-835. https://doi.org/10.1016/j.compag.2019.05.032.
Ha, P. T.; He, R.; Killiny, N.; Brown, J. K.; Omsland, A.; Gang, D. R. and Beyenal, H. 2019. Host-free biofilm culture of “Candidatus liberibacter asiaticus” the bacterium associated with Huanglongbing. Biofilm. 1(1):100005. https://doi.org/10.1016/j.bioflm.2019.100005.
He, C.; Li, X.; Liu, Y.; Yang, B.; Wu, Z.; Tan, S.; Ye, D. and Weng, H. 2022. Combining multicolor fluorescence imaging with multispectral reflectance imaging for rapid citrus Huanglongbing detection based on lightweight convolutional neural network using a handheld device. Comput. Electron. Agric. 194(3):106808. https://doi.org/10.1016/j.compag.2022.106808.
Hindson, B. J.; Ness, K. D.; Masquelier, D. A.; Belgrader, P.; Heredia, N. J.; Makarewicz, A. J.; Bright, I. J.; Lucero, M. Y.; Hiddessen, A. L. and Legler, T. C. 2011. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal. Chem. 83(22):8604-8610. https://doi.org/10.1021/ac202028g.
Hong, Y.; Luo, Y.; Yi, J.; He, L.; Dai, L.; and Yi, T. 2019. Screening nested-PCR primer for ‘Candidatus Liberibacter asiaticus’ associated with citrus Huanglongbing and application in Hunan, China. 14(2):1-15. https://doi.org/10.1371/journal.pone.0212020.
Jagoueix, S.; Bové J. M. and Garnier, M. 1996. PCR detection of the two ‘Candidatus’ Liberibacter species associated with greening disease of citrus. Mol. Cell. Probes 10(1):43-50. https://doi.org/10.1006/mcpr.1996.0006.
Lafleche, D. and Bové, J. M. 1970. Mycoplasmes dans les agrumes atteints de “greening”, de stubborn, on des maladies similaires. Fruits. 25(6):455-465. https://agritrop.cirad.fr/421918/.
Li, W.; Hartung, J. S. and Levy, L. 2009. Quantitative real time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. J. Microbiol. Methods. 66(1):104-115. https://doi.org/10.1016/j.mimet.2005.10.018.
Lin, H.; Chen, C.; Doddapaneni, H.; Duan, Y.; Civerolo, E. L.; Bai, X. and Zhao, X. 2010. A new diagnostic system for ultra-sensitive and specific detection and quantification of Candidatus Liberibacter asiaticus, the bacterium associated with citrus Huanglongbing. J. Microbiol. Methods. 81(1):17-25. https://doi.org/10.1016/j.mimet.2010.01.014.
Manjunath, K. L.; Halbert, S. E.; Ramadugu, C.; Webb, S. and Lee, R. F. 2008. Detection of ‘Candidatus Liberibacter asiaticus’ in Diaphorina citri and its importance in the management of citrus huanglongbing in florida. Phytopathology. 98(4):387-396. https://doi.org/10.1094/phyto-98-4-0387.
Morgan, J. K.; Zhou, L.; Li, W.; Shatters, R. G.; Keremane, M. and Duan, Y. P. 2012. Improved real-time PCR detection of ‘Candidatus Liberibacter asiaticus’ from citrus and psyllid hosts by targeting the intragenic tandem-repeats of its prophage genes. Mol. Cell. Probes. 26(2):90-98. https://doi.org/10.1016/j.mcp.2011.12.001.
Nauman, M.; Umar, U. U. D.; Naqvi, S. A. H.; Rehman, A. U.; Malik, M. T.; Shahid, M.; Akbar, M. and Umair, M. 2021. Impact of improved DNA extraction method from citrus leaves midrib and PCR for the detection of citrus greening (Candidatus Liberibacter). Pakistan. J. Phytopatol. 33(1):161-170. https://doi.org/10.33866/phytopathol.033.01.0671.
Neupane, K. and Baysal-Gurel, F. 2021. Automatic identification and monitoring of plant diseases using unmanned aerial vehicles: a review. Remote sens. 13(19):1-23. https:// doi.org/10.3390/rs1319384.
NAPPO. 2012. North american plant protection organization. Secretariat of the north american plant protection organization. https://nappo.org/application/files/6515/8322/7229/NAPPO-HLB-DP-2-2012-04-10-e.pdf.
Oppert, B.; Stoss, S.; Monk, A. and Smith, T. 2019. Optimized extraction of insect genomic dna for long read sequencing. Methods and Protocols. 2(4):1-7. https://doi.org/10.3390/mps2040089.
Paredes-Tomás, C.; Luis-Pantoja, M.; Collazo-Cordero, C.; Peña-Bárzaga, I.; López-Hernández, D.; Batista-Le Riverend, L.; y Hernández-Rodríguez, L. 2015. Diferencias en la manifestación de síntomas asociados a la enfermedad Huanglongbing (HLB) en diferentes especies cítricas en Cuba. CitriFrut. 32(2):36-41.
Parker, J. K.; Wisotsky, S. R.; Johnson, E. G.; Hijaz, F. M.; Killiny, N.; Hilf, M. E. and Fuente, L. 2014. Viability of ‘Candidatus Liberibacter asiaticus’ prolonged by addition of citrus juice to culture medium. Phytopathology. 104(1):15-26. https://doi.org/10.1094/phyto-05-13-0119-r.
Ponce, L.; Etxeberria, E.; Gonzalez, P.; Ponce, A. and Flores, T. 2018. Rapid identification of huanlongbing-infected citrus plants using laser induced breakdown spectroscopy of phloem samples. Appl. Opt. 57(30):8841-8844. https://doi.org/10.1364/ao.57.008841.
Ranulfi, A. C.; Cardinali, M. C. B.; Kubota, T. M. K.; Freitas-Astúa, J.; Ferreira, E. J.; Bellete, B. S.; Silva, M. F. G. F.; Villas Boas, P. R.; Magalhães, A. B. and Milori, D. M. B. P. 2016. Laser induced fluorescence spectroscopy applied to early diagnosis of citrus huanglongbing. biosyst. Eng. 144(4):133-144. https://doi.org/10.1016/j.biosystemseng.2016.02.010.
Roistacher, C. N. 1991. Graft-transmissible diseases of citrus. Handbook for detection and diagnosis. FAO, Rome, Italy. 193-261 pp.
Sechler, A.; Schuenzel, E. L.; Cooke, P.; Donnua, S.; Thaveechai, N.; Postnikova, E.; Stone, A. L.; Schneider, W. L.; Damsteegt, V. D. and Schaad, N. W. 2009. Cultivation of ‘Candidatus Liberibacter asiaticus’, ‘Ca. L. africanus’, and ‘Ca. L. americanus’ associated with Huanglongbing. Phytopathology. 99(5):480-486. https://doi.org/10.1094/phyto-99-5-0480.
SENASICA. 2012. Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria. 2012. Protocolo para establecer áreas regionales de control del huanglongbing y el psílido asiático de los cítricos (ARCOs). 3, 24-27, 41-42 pp. http://www.siafeson.com/sitios/simdia/docs/protocolos/ProtocoloparaestablecerAreasRegionalesARCOSDICIEMBRE2012.pdf.
SENASICA. 2019. Servicio nacional de sanidad, inocuidad y calidad agroalimentaria. ficha técnica huanglongbing ‘Candidatus Liberibacter spp.’ Servicio nacional de sanidad, inocuidad y calidad agroalimentaria dirección general de sanidad vegetal. 5-9 pp.
SIAP. 2022. Servicio de Información Agroalimentaria y Pesquera. Anuario estadístico de la producción agrícola. https://nube.siap.gob.mx/cierreagricola/.
Syed-Ab-Rahman, S. F.; Hesamian, M. H. and Prasad, M. 2022. Citrus disease detection and classification using end-to-end anchor-based deep learning model. Appl. Intell. 52(1):927-938. https://doi.org/10.1007/s10489-021-02452-w.
Teixeira, D. C.; Danet, J. L.; Eveillard, S.; Martins, E. C.; Jesus-Junior, W. C.; Yamamoto, P. T.; Aparecido-Lopes, S.; Beozzo-Bassanezi, R.; Ayres, A. J.; Saillard, C. and Bové, J. M. 2005. Citrus huanglongbing in São Paulo State, Brazil: PCR detection of the ‘Candidatus’ Liberibacter species associated with the disease. Mol. Cell. Probes. 19(3):173-179. https://doi.org/10.1016/j.mcp.2004.11.002.
Teixeira, D. D. C.; Wulff, N. A.; Martins, E. C.; Kitajima, E. W.; Bassanezi, R.; Ayres, A. J.; and Bové, J. M. 2008. A phytoplasma closely related to the pigeon pea witches’-broom phytoplasma (16sr ix) is associated with citrus Huanglongbing symptoms in the state of São Paulo, Brazil. Phytopathology. 98(9):977-984.
Wetterich, C. B.; Felipe de Oliveira, N. R.; Belasque, J.; Ehsani, R. and Marcassa, L. G. 2017. Detection of huanglongbing in florida using fluorescence imaging spectroscopy and machine-learning methods. Appl. Opt. 56(1):15-23. https://doi.org/10.1364/ao.56.000015.
Xu, Q.; Cai, J.; Zhang, W.; Bai, J.; Li, Z.; Tan, B. and Sun, L. 2022. Detection of citrus Huanglongbing (HLB) based on the HLB-induced leaf starch accumulation using a home-made computer vision system. Biosyst. Eng. 218(6):163-174. https://doi.org/10.1016/j.biosystemseng.2022.04.018.
Xue, A.; Liu, Y.; Li, H.; Cui, M.; Huang, X.; Wang, W.; Wu, D.; Guo, X.; Hao, Y. and Luo, L. 2022. Early detection of huanglongbing with EESI-MS indicates a role of phenylpropanoid pathway in citrus. Anal. Biochem. 639(4):114511. https://doi.org/10.1016/j.ab.2021.114511.
Yang, Y.; Zhou, Q.; Zahr, K.; Harding, M. W.; Feindel, D. and Feng, J. 2021. Impact of DNA extraction efficiency on the sensitivity of PCR based plant disease diagnosis and pathogen quantification. Eur. J. Plant Pathol. 159(3):583-591. https://doi.org/10.1007/s10658-020-02189-1.
Yang, P.; Nie, Z. and Yao, M. 2022. Diagnosis of HLB-asymptomatic citrus fruits by element migration and transformation using laser induced breakdown spectroscopy. Opt. Express. 30(11):18108. https://doi.org/10.1364/oe.454646.
Yzquierdo-Alvarez, M. E.; Ortiz-García, C. F. and Rincón-Ramírez, J. A. 2022. Detection of huanglongbing of citruses (Citrus sp.) through Sentinel 2satellite images in Huimanguillo, Tabasco, México. Agro Productividad. https://doi.org/10.32854/agrop.v14i12.2053.
Zhong, X.; Liu, X. L.; Lou, B. H.; Zhou, C. Y. and Wang, X. F. 2018. Development of a sensitive and reliable droplet digital PCR assay for the detection of ‘Candidatus Liberibacter asiaticus’. J. Integr. Agric. 17(2):483-487. https://doi.org/10.1016/S2095-3119(17)61815-X.
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