African Journal of
Plant Science

  • Abbreviation: Afr. J. Plant Sci.
  • Language: English
  • ISSN: 1996-0824
  • DOI: 10.5897/AJPS
  • Start Year: 2007
  • Published Articles: 807

Review

Alleviation of Huanglongbing disease in citrus by foliar application of microelements

Inoue Haruhiko
  • Inoue Haruhiko
  • Division of Plant Molecular Regulation, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki, 305-8605, Japan.
  • Google Scholar
Masaoka Yoshikuni
  • Masaoka Yoshikuni
  • Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan.
  • Google Scholar


  •  Received: 28 February 2022
  •  Accepted: 19 July 2022
  •  Published: 31 August 2022

References

Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-ur-Rehman M, Irshad MK, Bharwana SA (2015). The effect of excess copper on growth and physiology of important food crops: a review. Environmental Science and Pollution Research 22(11):8148-8162.
Crossref

 

Azrag AG, Mohamed SA, Khamis FM, Rasowo BA, Ambajo J, Sétamou M, Ekesi S, Borgemeister C (2021). Temperature-based phenology model of African citrus triozid (Trioza erytreae Del Guercio): Vector of citrus greening disease. Journal of Applied Entomology 146(1-2):88-97.
Crossref

 

Ajene IJ, Khamis F, van Asch B, Pietersen G, Rasowo BA, Ekesi S, Mohammed S (2020). Habitat suitability and distribution potential of Liberibacter species ("Candidatus Liberibacter asiaticus" and "Candidatus Liberibacter africanus") associated with citrus greening disease. Diversity and Distributions 26(5):575-588.
Crossref

 

Albrecht U, Bowman KD (2008). Gene expression in Citrus sinensis (L.) Osbeck following infection with the bacterial pathogen Candidatus Liberibacter asiaticus causing Huanglongbing in Florida. Plant Science 175(3):291-306.
Crossref

 

Aritua V, Achor D, Gmitter FG, Albrigo G, Wang N (2013). Transcriptional and microscopic analyses of citrus stem and root responses to Candidatus Liberibacter asiaticus infection. PLoS One 8:e73742.
Crossref

 

Aubert B, Quilici S (1984). Biological control of the African and Asian citrus psyllids (Homoptera: Psylloidea), through eulophid and encyrtid parasites (Hymenoptera: Chalcidoidea) in Reunion Island. In International Organization of Citrus Virologists Conference Proceedings (1957-2010) 9(9).
Crossref

 

Aznar A, Chen NW, Thomine S, Dellagi A (2015). Immunity to plant pathogens and iron homeostasis. Plant Science 240:90-97.
Crossref

 

Bakshi S, He ZL, Harri, WG (2013). Particulate copper in soils and surface runoff from contaminated sandy soils under citrus production. Environmental Science and Pollution Research 20(12):8801-8812.
Crossref

 

Bassanezi RB, Belasque Jr J, Montesino LH (2013). Frequency of symptomatic trees removal in small citrus blocks on citrus huanglongbing epidemics. Crop Protection 52:72-77.
Crossref

 

Bassanezi RB, Lopes SA, Miranda MP, Wulff NA, Volpe HXL, Ayres AJ (2020). Overview of citrus huanglongbing spread and management strategies in Brazil. Tropical Plant Pathology 45(3):251-264.
Crossref

 

Bassanezi RB, Montesino LH, Gasparato AB, Filho B, Amorim L (2011). Yield loss caused by Huanglongbing in different sweet orange cultivars in Brazil. European Journal of Plant Pathology 130(4):577-586.
Crossref

 

Behlau F, Belasque Jr J, Graham JH, Leite Jr RP (2010). Effect of frequency of copper applications on control of citrus canker and the yield of young bearing sweet orange trees. Crop Protection 29(3):300-305.
Crossref

 

Bové JM (2006). Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88:7-37.

 

Bové JM (2012). Huanglongbing and the future of citrus in Sao Paulo State, Brazil. Journal of Plant Pathology 94:465-467.

 

Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007). Zinc in plants. New Phytology 173:677-702.
Crossref

 

Camp AF, Fudge BR (1939). Some symptoms of citrus malnutrition in Florida. Florida Agricultural Experiment Station Bulletin 335:8-16.

 

Castle WS, Nunnallee J, Manthey JA (2009). Screening citrus rootstocks and related selections in soil and solution culture for tolerance to low-iron stress. HortScience 44(3):638-645
Crossref

 

Chanvatik S, Donnua S, Lekagul A, Kaewkhankhaeng W, Vongmongkol V, Athipunyakom P, Khamlar S, Prommintara M, Tangcharoensathien V (2019). Antibiotic use in mandarin production (Citrus reticulata Blanco) in major mandarin-producing areas in Thailand: A survey assessment. PLoS One 14:e0225172.
Crossref

 

Chaves JA, Oliveira LM, Silva LC, Silva BN, Dias CS, Rios JA, Rodrigues FÁ (2021). Physiological and biochemical responses of tomato plants to white mold affected by manganese phosphite. Journal of Phytopathology 169(3):149-167.
Crossref

 

da Silva JR, de Alvarenga FV, Boaretto RM, Lopes JRS, Quaggio JA, Coletta Filho HD, Mattos D (2020). Following the effects of micronutrient supply in HLB-infected trees: plant responses and 'Candidatus Liberibacter asiaticus' acquisition by the Asian citrus psyllid. Tropical Plant Pathology 45(6):597-610.
Crossref

 

Driscoll PJ (2004). Copper toxicity on Florida citrus-Why did it happen? In Proceedings of the Florida State Horticultural Society 117:124-127.

 

Duan Y, Zhou L, Hall DG, Li W, Doddapaneni H, Lin H, Liu L, Vahling CM, Gabriel DW, Williams KP, Dickerman A (2009). Complete genome sequence of citrus huanglongbing bacterium, 'Candidatus Liberibacter asiaticus' obtained through metagenomics. Molecular Plant-Microbe Interactions 22(8):1011-1020.
Crossref

 

Ebel RC, Hamido S, Morgan KT (2019). Interaction of Huanglongbing and foliar applications of copper on growth and nutrient acquisition of Citrus sinensis cv. Valencia. HortScience 54(2):297-302.
Crossref

 

Fan J, He Z, Ma LQ, Stoffella PJ (2011). Accumulation and availability of copper in citrus grove soils as affected by fungicide application. Journal of Soils and Sediments 11(4):639-648.
Crossref

 

Fernando DR, Lynch JP (2015). Manganese phytotoxicity: new light on an old problem. Annals of Botany 116(3):313-319.
Crossref

 

Ghosh DK, Motghare M, Gowda S (2018). Citrus greening: Overview of the most severe disease of citrus. Journal of Advanced Agricultural Technologies 2(1):83-100.

 

Gottwald TR (2010). Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology 48:119-139.
Crossref

 

Gottwald TR, Graham JH, Irey MS, McCollum TG, Wood BW (2012). Inconsequential effect of nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress. Crop Protection 36:73-82.
Crossref

 

Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013). Biology and management of Asian Citrus Psyllid, vector of the huanglongbing pathogens. Annual Review of Entomology 58(1):413-432.
Crossref

 

Graham J, Gerberich K, Bright D, Johnson E (2017). Soil and water acidification sustain root density of huanglongbing-infected trees in Florida. In Proceedings of the 5th International Research Conference on Huanglongbing, Orlando, FL, USA. pp. 14-17.

Crossref

 

Haydon MJ, Cobbett CS (2007). Transporters of ligands for essential metal ions in plants. New Phytology 174(3):499-506.
Crossref

 

Hu J, Jiang J, Wang N (2018). Control of citrus Huanglongbing via trunk injection of plant defense activators and antibiotics. Phytopathology 108(2):186-195.
Crossref

Huang CY, Araujo K, Sánchez JN, Kund G, Trumble J, Roper C, Godfrey KE, Jin H (2021). A stable antimicrobial peptide with dual functions of treating and preventing citrus Huanglongbing. Proceedings of the National Academy of Sciences of the USA 118:e2019628118.

Hussain Z, Iftikhar Y, Mubeen M, Saleem MZ, Naseer MU, Luqman M, Abbas A (2022). Application of micronutrients enhances the quality of kinnow mandarin infected by citrus greening disease (Huanglongbing). Sarhad Journal of Agriculture 38(1):360-371.
Crossref

 

Inoue H, Okada A, Uenosono S, Suzuki M, Matsuyama T, Masaoka Y (2020b). Does HLB disease prefer citrus growing in alkaline soil? Japan Agricultural Research Quarterly 54(1):21-29.
Crossref

 

Inoue H, Yamashita-Muraki S, Fujiwara K, Honda K, Ono H, Nonaka T, Kato Y, Matsuyama T, Sugano S, Suzuki M, Masaoka Y (2020a). Fe2+ ions alleviate the symptom of citrus greening disease. International Journal of Molecular Sciences 21:4033.
Crossref

 

Irey MS, Gast T, Snively J (2008). Economic impact of managing huanglongbing in groves at Southern Gardens citrus. In International Workshop of Huanglongbing and the Asian Citrus Psyllid. Clewiston, FL. Available at:

View

 

Jagoueix S, Bove JM, Garnier M (1994). The phloem-limited bacterium of greening disease of citrus is a member of the α subdivision of the Proteobacteria. International Journal of Systematic and Evolutionary Microbiology 44(3):379-386.
Crossref

 

Kalim S, Luthra YP, Gandhi SK (2003). Role in zinc and manganese in resistance of cowpea root rot. Journal of Plant Diseases and Protection 110:235-243.

 

Kopittke PM, Menzies NW (2006). Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant and Soil 279(1):287-296.
Crossref

 

Kwakye S, Kadyampakeni DM, van Santen E, Vashisth T, Wright A (2022). Variable Manganese Rates Influence the Performance of Huanglongbingaffected Citrus Trees in Florida. Hortscience 57(3):360-366.
Crossref

 

Li S, Wu F, Duan Y, Singerman A, Guan Z (2020). Citrus greening: Management strategies and their economic impact. HortScience 55(5):604-612.
Crossref

 

Ma Z, Jacobsen FE, Giedroc DP (2009). Metal transporters and metal sensors: How coordination chemistry controls bacterial metal homeostasis. Chemical Reviews 109(10):4644.
Crossref

 

Manzanilla-Ramírez MÁ, Villegas-Monter Á, Velázquez-Monreal JJ, Zavaleta-Manceral HA, Sandoval-Villal M, Muñoz-Orozco A (2019). Physiological changes in Mexican lemon trees in production infected with HLB. Revista Mexicana de Ciencias Agrícolas 10(7):1063-1614.
Crossref

 

Marschner H (2011). Marschner's Mineral Nutrition of Higher Plants. Academic press: London.

 

Masaoka Y, Pustika A, Subandiyah S, Okada A, Hanundin E, Purwanto B, Okuda M, Okada Y, Saito A, Holford P, Beattie A (2011). Lower concentrations of microelements in leaves of citrus infected with 'Candidatus Liberibacter asiaticus.' Japan Agricultural Research Quarterly 45(3):269-275.
Crossref

 

McDevitt CA, Ogunniyi AD, Valkov E, Lawrence MC, Kobe B, McEwan AG, Paton JC (2011). A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathogens 7:e1002357.
Crossref

 

McKenna M (2019). Antibiotics set to flood Florida's troubled orange orchards. Nature 567(7748):302-304.
Crossref

 

Mesquita GL, Tanaka FA, Zambrosi FC, Chapola R, Cursi D, Habermann G, Massola Jr NS, Ferreira VP, Gaziola SA, Azevedo RA (2019). Foliar application of manganese increases sugarcane resistance to orange rust. Plant Pathology 68(7):1296-1307.
Crossref

 

Miyakawa T, Tsuno K (1989). Occurrence of citrus greening disease in the southern islands of Japan. Japan Journal of Phytopathology 55(5):667-670.
Crossref

 

Morgan KT, Rouse RE, Ebel RC (2016). Foliar applications of essential nutrients on growth and yield of 'Valencia' sweet orange infected with Huanglongbing. HortScience 51(12):1482-1493.
Crossref

 

Mori S (1999). Iron acquisition by plants. Current Opinion in Plant Biology 2(3):250-253.
Crossref

 

Naito T, Taba S, Toyosato T, Kawano S, Takaesu K, Uehara K (2001). Detection of the citrus Huanglongbing (greening disease) by polymerase chain reaction (PCR) assays and distribution in Okinawa, Japan. Bulletin of the Okinawa Agricultural Experiment Station 23:74-81.

 

Nobori T, Velásquez AC, Wu J, Kvitko BH, Kremer JM, Wang Y, He SY, Tsuda K (2018). Transcriptome landscape of a bacterial pathogen under plant immunity. Proceedings of the National Academy of Sciences of the USA 115:E3055-E3064.
Crossref

 

Nwugo CC, Lin H, Duan Y, Civerolo EL (2013). The effect of 'Candidatus Liberibacter asiaticus' infection on the proteomic profiles and nutritional status of pre-symptomatic and symptomatic grapefruit (Citrus paradisi) plants. BMC Plant Biolology 13(1):59.
Crossref

 

Ohtsu Y, Nakashima K, Prommintara M, Tomiyasu Y (1998). Typical symptoms of citrus greening on mandarin trees in Nepal, supported by detection and characterization of ribosomal DNA of the causal organisms. Japanese Journal of Phytopathology 64(6):539-545.
Crossref

 

Pérez CD, Pozza EA, Pozza AA, Elmer WH, Pereira AB, Guimarães DD, Monteiro AC, de Rezende ML (2020). Boron, zinc and manganese suppress rust on coffee plants grown in a nutrient solution. European Journal of Plant Pathology 156(3):727-738.
Crossref

 

C, Serra-Cardona A, Sánchez-Sanuy F, Campo S, Ariño J, San Segundo B (2017). Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice. Molecular Plant-Microbe Interactions 30(5):385-398.
Crossref

 

Ramadugu C, Keremane ML, Halbert SE, Duan YP, Roose ML, Stover E, Lee RF (2016). Long-term field evaluation reveals Huanglongbing resistance in Citrus relatives. Plant Disease 100(9):1858-1869.
Crossref

 

Rasowo BA, Khamis FM, Mohamed SA, Ajene IJ, Aidoo OF, Ombura L, Sétamou M, Ekesi S, Borgemeister C (2019). African citrus greening disease in East Africa: Incidence, severity, and distribution patterns. Journal of Economic Entomology 112(5):2389-2397.
Crossref

 

Razi MF, Khan IA, Jaskani MJ (2011). Citrus plant nutritional profile in relation to Huanglongbing prevalence in Pakistan. Pakistan Journal of Agricultural Sciences 48(4):299-304.

 

Römheld V, Marschner H (1986). Evidence for a specific uptake system for iron phytosiderophores in roots ofgrasses. Plant Physiology 80(1):175-180.
Crossref

 

Shahzad F, Chun C, Schumann A, Vashisth T (2020). Nutrient uptake in huanglongbing-affected sweet orange: Transcriptomic and physiological analysis. Journal of the American Society for Horticultural Science 145(6):349-362.
Crossref

 

Shi G, Zhang Z, Friesen TL, Raats D, Fahima T, Brueggeman RS, Lu S, Trick HN, Liu Z, Chao W, Frenkel Z (2016). The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Science Advances 2:e1600822.
Crossref

 

Singerman A, Useche P (2016). Impact of citrus greening on citrus operations in Florida. University of Florida/Institute of Food and Agricultural Sciences Extension. FE983.?

 

Tian S, Lu L, Labavitch JM, Webb SM, Yang X, Brown PH, He Z (2014). Spatial imaging of Zn and other elements in Huanglongbing-affected grapefruit by synchrotron-based micro X-ray fluorescence investigation. Journal of Experimental Botany 65(4):953-964.
Crossref

 

Vahling-Armstrong CM, Zhou H, Benyon L, Morgan JK, Duan Y (2012). Two plant bacteria, and. Liberibacter asiaticus, share functional znuABC homologues that encode for a high affinity zinc uptake system. PLoS One 7:e37340.
Crossref

 

Wang N (2019). The citrus huanglongbing crisis and potential solutions. Molecular Plant 12(5):607-609.
Crossref

 

Wulandari C, Muraki S, Hisamura A, Ono H, Honda K, Kashima T, Subandiyah S, Masaoka Y (2014). Effect of iron deficiency on root ferric chelate reductase, proton extrusion, biomass production and mineral absorption of citrus root stock orange jasmine (Murraya exotica L.). Journal of Plant Nutrition 37(1):50-64.
Crossref

 

Yang C, Powell CA, Duan Y, Ancona V, Huang J, Zhang M (2020). Transcriptomic analysis reveals root metabolic alteration and induction of huanglongbing resistance by sulphonamide antibiotics in huanglongbing?affected citrus plants. Plant Pathology 69(4):733-743.
Crossref

 

Zambon FT, Kadyampakeni DM, Grosser JW (2019). Ground application of overdoses of manganese have a therapeutic effect on sweet orange trees infected with Candidatus Liberibacter asiaticus. HortScience 54(6):1077-1086.
Crossref

 

Zapata SD, Peguero F, Sétamou M, Alabi OJ (2021). Economic implications of citrus greening disease management strategies. Journal of Agricultural and Resource Economics 47(2):300-323.

 

Zhang L, Yao J, Withers J, Xin XF, Banerjee R, Fariduddin Q, Nakamura Y, Nomura K, Howe GA, Boland W, Yan H (2015). Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor. Proceedings of the National Academy of Sciences of the USA 112(46):14354-14359.
Crossref

 

Zhang M, Guo Y, Powell CA, Doud MS, Yang C, Duan Y (2014). Effective antibiotics against 'Candidatus Liberibacter asiaticus' in HLB-affected citrus plants identified via the graft-based evaluation. PLoS One 9:e111032.
Crossref

 

Zhang M, Karuppaiya P, Zheng D, Sun X, Bai J, Ferrarezi RS, Duan Y (2021). Field evaluation of chemotherapy on HLB-affected citrus trees with emphasis on fruit yield and quality. Frontiers in Plant Science 12:611287.
Crossref

 

Zhang MQ, Guo Y, Powell CA, Doud MS, Yang CY, Zhou H, Duan YP (2016). Zinc treatment increases the titre of 'Candidatus Liberibacter asiaticus' in huanglongbing?affected citrus plants while affecting the bacterial microbiomes. Journal of Applied Microbiology 120(6):1616-1628.
Crossref

 

Zhong Y, Cheng CZ, Jiang NH, Jiang B, Zhang YY, Wu B, Hu ML, Zeng JW, Yan HX, Yi GJ, Zhong GY (2015). Comparative transcriptome and iTRAQ proteome analyses of citrus root responses to Candidatus Liberibacter asiaticus infection. PLoS One 10:e0126973.
Crossref