Evaluation of susceptibility of ten Citrus Genotypes to ‘Candidatus Liberibacter asiaticus’ the causal agent of citrus greening.

Document Type : Research paper-Persian

Authors

1 PhD student of Plant Pathology, Department of Plant Pathology, Faculty of Agriculture, Varamin-Pishva Branch, Islamic Azad University, Varamin, Tehran, Iran

2 Associate Professor, Plant Protection Research Department, Iranian Research Institute of Plant Protection (IRIPP), Agricultural Research,Education and Extension Organization (AREEO) Tehran, Iran

3 Assistant Professor, Plant Protection Research Department, Fars Agricultural and Natural Resources Research and Education Center, AREEO, Zarghan, Iran

4 Assistant Professor, Department of Industrial and Environmental Biotechnology, National Institute of Genetic engineering and Biotechnology, NIGEB, Tehran, Iran

5 Assistant Professor, Department of Plant Pathology, Faculty of Agriculture, Varamin-Pishva Branch, Islamic Azad University, Varamin, Tehran, Iran

Abstract

Background and Objectives
Citrus greening (HLB) is one of the most damaging citrus diseases worldwide. As well, the three most important causal agents of this disease in the world include "Candidatus (Ca.) Liberibacter asiaticus ("CLas"), Ca. Liberibacter africanus ("CLaf"), and Ca. Liberibacter americanus ("CLam"). Accordingly, these were reported from Asian-American, African, and American countries, respectively. Of note, "CLas" species is found as the most important causal agent of this disease in all countries in the world, including Iran. It seems that the most effective way to reduce HLB is finding those cultivars that are resistant or tolerant to HLB. Accordingly, in the present study, an attempt was made to evaluate the reaction of a number of common citrus cultivars to this bacterium.
Materials and Methods
In the present research, ten commercial rootstocks and cultivars of the common citrus in the south of Iran, including Mexican lime, sour orange, mandarin orange, Kinnow mandarin, Orlando tangelo mandarin, local orange, Valencia orange ,sweet lemon, grapefruit, and Lisbon lemons were prepared as seedlings. After checking their health, they were inoculated with the citrus greening agent and then kept in an insect-free greenhouse at night at 25°C and during the day at 30°C.By passing two months from the inoculation, the pathogen was detected by performing specialized tests in inoculated seedlings. Thereafter, three two-year-old seedlings from each one of the above-mentioned rootstocks and cultivars were grafted with two infected buds. Two months after the inoculation, normal and nested PCR tests were performed on the vein tissue extract of the infected seedlings, once every two months, for a 12-month duration. Finally, both sensitivity and relative resistance of cultivars were evaluated based on the average number of days until the detection of the first Ca. L. asiaticus by PCR and also the incubation period of the disease, in each seedling.
Results
The causal agent of this disease ("CLas") was detected at the earliest time(in Valencia oranges and Orlando tangelo mandarin after 180 and 200 days, respectively) after the inoculation with infected graft, compared to other cultivars and rootstocks. Among the studied species, the "CLas" was detected in both Mexican lime and Lisbon lemon with the longest delay (by passing 330 and 300 days from the inoculation, respectively). According to the results, "CLas" was detected in sour orange and sweet lemon 290 and 280 days after the inoculation with infected graft, respectively. Based on the average number of days until the detection of the first Ca. L. asiaticus by PCR and also the incubation period of the disease, in each seedling, Mexican lime and Lisbon lemon were found as the most tolerant species and Valencia oranges and Orlando tangelo mandarin were found as the most susceptible ones to HLB. Moreover, sour orange and sweet lemon seedlings were moderately susceptible ones; and grapefruit, local orange, local, and Kinnow mandarin were moderately tolerant to HLB.
Discussion
Due to the reason that this bacterium does not grow in conventional medium, in this study, it was not possible to multiply it in artificial medium and then contaminate the plant with it. Therefore, performing the inoculation through grafting the seedlings with HLB infected buds was considered as the most appropriate method for seedlings inoculation with the pathogen. The faster the pathogen can settle and multiply and the symptoms appear in the host, the greater the susceptibility of the host to the disease. Early pathogen’s detection and symptoms’ observation in some hosts such as Valencia oranges and Orlando tangelo mandarin, indicate better bacterial proliferation in both cultivars. Notably, no symptoms of the disease were observed in Mexican lime and Lisbon lemons after 15 months, and one year after the inoculation in sour orange and sweet lemon plants. There is evidence that all known citrus cultivars are affected to this pathogen with different degrees of susceptibility. Based on the results of this study and the results of previous researchers in the world, it seems that researchers should look for the sources of resistance factors to HLB in more species and cultivars. Correspondingly, these sources can be used in the following two ways: used as a rootstock or scion, and used in the efforts of breeders to produce a resistant cultivar.

Keywords

References

Albrecht, U., Hall, D.G. & Bowman, K.D. (2014). Transmission efficiency of ‘Candidatus Liberibacter asiaticus’ and progression of huanglongbing disease in graft and psyllid-inoculated citrus. HortScience, 49: 367-377.
Alizadeh Aliabadi, A. (2003). Biological attacks on agricultural products. a new challenge to plant protection. Plant Protection Organization of Iran. Agricultural Education Publication, (105 pp.) (In Persian with English summary).
Alizadeh Aliabadi, A. (2004). Citrus Greening: a serious threat to citrus orchards and nurseries of Iran. Olive Journal, 205: 14-8. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2009). Citrus Greening caused by Candidatus Liberibacter spp. Iranian Research Institute of Plant Protection. Agricultural Research. Education and Extension Organization. Agricultural Education Publication, 232 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2017)a. Detection of citrus greening disease in citrus orchards and nurseries of Iran. Iranian Research Institute of Plant Protection. Agricultural Research. Education and Extension Organization. Agricultural Education Publication, 32 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2017)b. How to collect and identify infected plants with citrus Greening disease. Iranian Research Institute of Plant Protection. Agricultural Research, Education and Extension Organization. Agricultural Education Publication. 24 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2017)c. Production of healthy seedlings free from citrus greening agent. Iranian Research Institute of Plant Protection. Agricultural Research. Education and Extension Organization. Agricultural Education Publication, 20 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2017)d. Removal methods of infected citrus greening trees. Iranian Research Institute of Plant Protection. Agricultural Research. Education and Extension Organization. Agricultural Education Publication. 20 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. & Ghasemi, A. (2018). Detection of greening agent bacteria in the body of the Asian citrus psyllid Diaphorina citri Kuwayama in Orzuieh, Jiroft and Kahnooj regions. Iranian Research Institute of Plant Protection. Agricultural Research, Education and Extension Organization. (Research Report No. 53336), 26 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A. (2016). Integrated Citrus Greening Management National Project. Iranian Research Institute of Plant Protection. Agricultural Research, Education and Extension Organization. (Research Report No. 51301), 180 pp. (In Farsi with English summary).
Alizadeh Aliabadi, A., Foroutan, A. & Golmohamadi, M. (2010). Occurrence of citrus greening caused by Candidatus Liberibacter asiaticus in Sistan-Baluchestan province. 19th Iranian Plant Protection Congress. 31 July-3 August (2010). Tehran. IRAN. p. 525. (In Farsi with English summary).
Alizadeh Aliabadi, A., Ghasemi, A., Salehi, M., Faqihi, M.M. & Forootan, A. (2013). Identification and distribution of citrus greening disease in Iran. Iranian Research Institute of Plant Protection. Agricultural Research, Education and Extension Organization. (Research Report No. 44237), 38 pp. (In Farsi with English summary).
Batool, A., Iftikhar, Y., Mughal, S.M., Khan, M.M., Jaskani, M.J., Abbas, M. & Khan, I.A. (2007). Citrus greening disease - A major cause of citrus decline in the world - A Review. Horticultural Science, 34(4): 159-166.
Bhagabati, K.N. (1993). Survey of greening disease of mandarin orange in the northeastern states of India, (p. 441–442). In: Moreno, P., da Gracxa, J.V., & Timmer L.W. (eds.).. 12th International Organization of Citrus Virologists Conference Proceedings (IOCV), Riverside, CA.
Bové, J.M., Calavan, E.C., Capoor, S.P., Cortez, R.E. & Schwarz, R.E. (1974). Influence of temperature on symptoms of California stubborn, South African greening, Indian citrus decline and Philippines leaf mottling diseases. 6th International Organization of Citrus Virologists Conference Proceedings, pp. 12-15.
Bove, J.M. (2006). Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, 88: 7–37.
Canale, M.C., Komada, K. & Lopes, J.R.S. (2019). Latency and incubation of ‘Candidatus Liberibacter asiaticus’ in citrus after vector inoculation. Tropical Plant Pathology, 45: 320-326.
Canale, M.C., Tomaseto, A.F., Haddad, M.D.L., Lopes, J.R.S. & Filho, H.D.C. (2017). Latency and Persistence of “Candidatus Liberibacter asiaticus” in its Psyllid Vector, Diaphorina citri Kuwayama (Hemiptera: Liviidae). Phytopathology, 107: 264–272.
Coletta-Filho H.D., Targon M.L.P.N., Takita M.A., De Negri J.D., Pompeu, J.J. & Machado, M.A. (2004). First Report of the Causal Agent of Huanglongbing (“Candidatus Liberibacter asiaticus”) in Brazil. Plant Disease, 88: 1382.
Coletta-Filho, H.D., Daugherty, M.P., Ferreira, C. & Lopes, J.R.S. (2014). Temporal Progression of “Candidatus Liberibacter asiaticus” Infection in Citrus and Acquisition Efficiency by Diaphorina citri. Phytopathology, 104: 416-421.
Da Graça, J. V. (2008). Biology, history and world status of huanglongbing. Hermosillo, Sonora. México. Texas A & M University-Kingsville, Citrus Center, Weslaco TX 78596, USA. 7pp.
Da Graca, JV., Douhan, G.W., Halbert, SE., Keremane, ML., Lee, R.F. & Vidalakis, G. (2015). Huanglongbing: an overview of a complex pathosystem ravaging the world’s citrus. Journal of Integrative Plant Biology, 58: 373-387.
Faghihi, M., Salehi, M., Bagheri, A. & Izadpanah, K. (2009). First report of citrus huanglongbing disease on orange in Iran. Plant Pathology, 58: 793-793.
Folimonova, S.Y., Robertson, C.J., Garnsey, S.M., Gowda, S. & Dawson, W.O. (2009). Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology, 99: 1346-1354.
French, J.V., Kahlke, C. & da Graça, J.V. (2001). Asian psyllid found on Texas citrus. Citrus Center, 19: 1.
Gabriel, D., Gottwald, T.R., Lopes, S.A. & Wulff, N.A. (2020). Chapter 18: Bacterial pathogens of citrus: Citrus canker. citrus variegated chlorosis and Huanglongbing. In The Genus Citrus, Editor(s): Talon, M., Caruso, M., Gmitter, F. G. 2020. (pp. 371-38) Elsevier.
Garnier, M. & Bové, J.M. (1977). Structure trilamellaire des deux membranes qui entourent les organismes procaryotes associés à la maladie du “greening” des agrumes. Fruits, 32: 749-752.
Garnier, M., Danel, N. & Bové, J.M. (1984). Aetiology of Citrus Greening Disease. Annual of Microbiology (Institute Pasteur), 135A: 169-179.
Ghayeb zamharir, M., Alizadeh, A. & Kachoei, S. (2014)a. Phylogenetic analysis of divergent structural organization of nucleotide binding domain encoded by resistance genes and gene homologes in Citrus. International Journal of Agriculture and Crop Sciences, 77: 379-385.
Ghayeb Zamharir, M., Hamzeh, K., Alizadeh, A. & Kachoei, S. (2014)b. A Semiquantitative Rt-Pcr Assay To Evaluated The Expression Patterns Of Nbs-Lrr Family Genes In Infectedfected Citrus By Candidatus Leiberibacter Asiaticus. International Journal of Agriculture and Crop Sciences, Available online at: www.ijagcs.com.
Gholampour, H., Ghayeb Zamharir, M., Karimi, J., Farrokhi, N., Alizadeh, A. & Taheri, P. (2014). Identification of Genes Expressed Differentially in Grapefruit Infected with Candidatus Liberibacter asiaticus in the Late Stage of Disease. Journal of Phytopathology, 162: 811-819.
Gottwald, T.R. (2010). Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology, 48: 119-139.
Halbert, S.E. (2005). The discovery of huanglongbing in Florida. Proceedings Of 2nd International Citrus Canker and Huanglongbing Research Workshop, Florida Citrus Mutual, Orlando, H-3.
Halbert, S.E. & Nuñez, C.A. (2004). Distribution of the Asian citrus psyllid, Diaphorina citri Kuwayama (Rhynchota: Psyllidae) in the Caribbean basin. Florida Entomologist, 87: 401-402.
Halbert, S.E. & Manjunath, K.L. (2004). Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Florida Entomologist, 87: 330-353.
Hamzeh, K., Ghayeb Zamharir, M., Alizadeh, A. & Kachoei, S. (2014). Study of quantitative expression of citrus tristeza virus resistance gene homolouge in A., the infected citrus by citrus greening pathogen. Applied plant protection, 4: 12.
Hilf, M.E. & Lewis, R.S. (2016). Transmission and propagation of ‘Candidatus Liberibacter asiaticus’ by grafting with individual citrus leaves. Phytopathology, 106:452-458.
Hocquellet, A., Toorawa, P., Bove, J.M. & Garnier, M. (1999). Detection and identification of the two Candidatus liberobacter species associated with citrus huanglongbing by PCR amplification of ribosomal protein genes of the β operon. Molecular and Cellular Probes, 13: 373-9.
Hodges, AW., Spreen, TH., Rahmani, M., Stevens, T.J. & Spreen, T.H. (2015). Economic Impacts of Citrus Greening-HLB in Florida, 2006/07–2010/11. University of Florida's Institute of Food and Agricultural Sciences (UF/IFAS), pp 7-12.
Hung, T.H., Wu, M.L. & Su, H.J. (1999). Development of a rapid method for the diagnosis of citrus greening disease using the polymerase chain reaction. Journal of Phytopathology, 147: 599-604.
Irey, M.S., Gast, T. & Gottwald, T.R. (2006). Comparison of visual assessment and polymerase chain reaction assay testing to estimate the incidence of the huanglongbing pathogen in commercial Florida citrus. Proceedings of the Florida State Horticultural Society, 119: 89-93.
Jagoueix, S., Bové, J.M. & Garnier, M. (1994). The phloem-limited bacterium of greening disease of citrus is a member of the subdivision of the Proteobacteria. International Journal of Systematic Bacteriology, 44: 397-386.
Jagoueix, S., Bove, J.M. & Garnier, M. (1996). PCR detection of the two “Candidatus” liberobacter species associated with greening disease of citrus. Molecular and Cellular Probes, 10: 43-50.
Kumagai, L.B., LeVesque, C.S., Blomquist, C.L., Madishetty, K., Guo, Y. & Woods, P.W. (2012). First Report of Candidatus Liberibacter asiaticus Associated with Citrus Huanglongbing in California. Plant Disease, 97: 283.
Kunta, M., da Graça, J.V., Malik, N.S.A., Louzada, E.S. & Sétamou, M. (2014). Quantitative distribution of Candidatus Liberibacter asiaticus in the aerial parts of the Huanglongbing-infected citrus trees in Texas. Horticultural Science, 49: 65-68.
Li, Y., Xu, M., Dai, Z. & Deng, X. (2018). Distribution pattern and titer of Candidatus Liberibacter asiaticus in periwinkle (Catharanthus roseus). Journal of Integrative Agriculture, 17: 2501-2508.
McClean, A.P.D. & Schwarz, R.E. (1970). Greening or blotchy-mottle disease of citrus. Phytophylactica, 2: 177-194.
Miyakawa, T. (1980). Experimentally-induced symptoms and host range of citrus likubin (greening disease). Annals of the Phytopathological Society of Japan, 46: 224-230.
Miyakawa, T. & Zhao. X.Y. (1990). Citrus host range of greening disease, In: Aubert, B., S. Tontyaporn, & D. Buangsuwon (eds.). 4th International Asia Pacific Conference on Citrus Rehabilitation. FAO-UNDP, p. 118-121.
Moghbeli Gharaei, A., Ziaaddini, M. & Jalali, M.A. (2018). Olfactory responses of Diaphorina citri Kuwayama (Hem.: Psyllidae) to chemical compounds Gamma-butyrolactone and Methyl salicylate in laboratory conditions. Plant Protection (Scientific Journal of Agriculture), 41(1): 11-22. (In Farsi with English summary).
Mohkami, A., Sattari, R., Lori, Z., Ehsani, A. & Nazemi, A. (2011). First report of citrus huanglongbing in the Orzooiyeh region in Kerman province (Orzooiyeh). Iranian Journal of Plant Pathology, 47:105.
Muhammad, F.R., Khana, I.A., Jaskania, M.J. & Basrab, S.M.A. (2012). Graft transmission and biological indexing of huanglongbing on local citrus germplasm. Science International (Lahore), 24: 153-157.
Nariani, T.K. (1981). Integrated approach to control citrus greening disease in India. Proceedings of the International Society of Citriculture, 1: 471-472.
Ruangwong, O. & Akrapisan, A. (2006). Detection of Candidatus liberibacter asiaticus causing citrus Huanglongbing disease. Journal of Agricultural Technology, 2: 111-120.
Salehi, M., Faghihi, M., Khanchezar, A., Bagheree, A. & Izadpanah, K. (2012). Distribution of citrus Huanglongbing disease and its vector in southern Iran '. Iranian Journal of Plant Pathology. 48: 195-208. (In Farsi with English summary).
Schneider, H. (1968). Anatomy of greening-diseased sweet orange shoots. Phytopathology 58: 1155-1160.
Shokrollah, H.T., Abdullah, L., Sijam, K., Abdullah, S.N.A. & Abdullah, N.A.P. (2009). Differential reaction of citrus species in Malaysia to huanglongbing (HLB) disease using grafting method. American Journal of Agricultural and Biological Sciences, 4: 32-38.
Stover, E. & McCollum, G. (2011). Incidence and severity of huanglongbing and ‘Candidatus Liberibacter asiaticus’ titer among field-infected citrus cultivars. HortScience, 46: 1344-1348.
Teixeira, D., do Carmo Dane, J.L., Eveillard, S., Martins, E.C., Jesus Junior, W.C., de Yamamoto, P.T., Lopes, S.A., Bassanezi, R.B., Ayres, A.J., Saillard, C. & Bové, J.M. (2005). Citrus huanglongbing in São Paulo State, Brazil: PCR detection of the “Candidatus” Liberibacter species associated with the disease. Molecular Cellular Probes 19: 173-179.
Wang, N. & Trivedi, P. (2013). Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology, 103: 652-665.
Yosefi Hamedani, E., Sharifnabi, B. & Bahar, M. (2012). Rapid detection of armillaria mellea causal agent of root and crown rot in soil and wood samples by nested pcr method. Plant protection (Scientific Journal of Agriculture), 35(3): 71-82. (In Farsi with English summary).
Zhou, L.J., Gabriel, D.W., Duan, Y.P., Halbert, S.E. & Dixon, W.N. (2007). First report of dodder transmission of Huanglongbing from naturally infected Murraya paniculata to citrus. Plant disease, 91: 227.
© 2022 by the authors. Licensee SCU, Ahvaz, Iran. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0 license) (http://creativecommons.org/licenses/by-nc/4.0/).
Plant Protection (Scientific Journal of Agriculture)
Volume 44, Issue 4
January 2022
Pages 1-18

Files

Share

How to cite

Statistics