{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T17:45:09Z","timestamp":1778348709196,"version":"3.51.4"},"reference-count":56,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T00:00:00Z","timestamp":1613952000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>Huanglongbing (HLB) is one of the most devastating diseases of citrus, which is associated with <jats:italic>Candidatus<\/jats:italic> Liberibacter asiaticus (Las) in the United States. To date, no effective antimicrobial compound is commercially available to control the disease. In this study, we investigated the effects of different antimicrobial chemicals with suitable surfactants on HLB-affected matured citrus trees with emphasis on the fruit yield and quality. Each treatment was applied three times in a 2-week interval during the spring flush period, one time in summer and three times during the autumn flushing period. We extensively examined different parameters such as pathogenic index, disease index, tree canopy, fruit yield, quality, and nutritional status. The results showed that among the treatments, penicillin (PEN) with surfactant was most effective in suppressing Las titer in infected citrus trees, followed by Fosetyl-Al (ALI), Carvacrol (CARV), and Validamycin (VA). Fruit quality analysis revealed that PEN treatment increased the soluble solids content (SSC), whereas Oxytetracycline (OXY) treatment significantly reduced titratable acidity (TA) level and increased the SSC\/TA ratio compared to the control. Nutrient analysis showed increased N and Zn levels in ALI and PEN treatments, and OXY treatment increased leaf P, K, S, and Mg levels compared to untreated control. Furthermore, B, Ca, Cu, Fe, and Mn in leaves were reduced in all chemical treatments than that of the untreated control. These findings revealed that some of the chemical treatments were able to suppress Las pathogen, enhance nutritional status in leaves, and improve tree growth and fruit quality of HLB-affected trees.<\/jats:p>","DOI":"10.3389\/fpls.2021.611287","type":"journal-article","created":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T15:50:08Z","timestamp":1614009008000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Field Evaluation of Chemotherapy on HLB-Affected Citrus Trees With Emphasis on Fruit Yield and Quality"],"prefix":"10.3389","volume":"12","author":[{"given":"Muqing","family":"Zhang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Palaniyandi","family":"Karuppaiya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Desen","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiuxiu","family":"Sun","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinhe","family":"Bai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rhuanito S.","family":"Ferrarezi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Charles A.","family":"Powell","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yongping","family":"Duan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2021,2,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1104\/pp.108.133629","article-title":"Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots.","volume":"150","author":"Armengaud","year":"2009","journal-title":"Plant Physiol."},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.3390\/foods5010004","article-title":"Changes in volatile and non-volatile flavor chemicals of \u201cValencia\u201d orange juice over the harvest seasons.","volume":"5","author":"Bai","year":"2016","journal-title":"Foods"},{"key":"B3","doi-asserted-by":"publisher","first-page":"1100","DOI":"10.21273\/hortsci12000-17","article-title":"Effect of vector control and foliar nutrition on quality of orange juice affected by Huanglongbing: chemical analysis.","volume":"52","author":"Baldwin","year":"2017","journal-title":"HortScience"},{"key":"B4","doi-asserted-by":"publisher","first-page":"2877","DOI":"10.1021\/acs.jafc.7b05635","article-title":"Effect of abscission zone formation on orange (Citrus sinensis) fruit\/juice quality for trees affected by Huanglongbing (HLB).","volume":"66","author":"Baldwin","year":"2018","journal-title":"J. Agric. Food Chem."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1021\/jf9031958","article-title":"Effect of Liberibacter infection (Huanglongbing disease) of citrus on orange fruit physiology and fruit\/fruit juice quality: chemical and physical analyses.","volume":"58","author":"Baldwin","year":"2010","journal-title":"J. Agric. Food Chem."},{"key":"B6","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1007\/s10658-011-9779-1","article-title":"Yield loss caused by huanglongbing in different sweet orange cultivars in S\u00e3o Paulo.","volume":"130","author":"Bassanezi","year":"2011","journal-title":"Brazil. Eur. J. Plant Pathol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/j.scienta.2016.01.019","article-title":"Performance of \u2018Valencia\u2019orange (Citrus sinensis [L.] Osbeck) on 17 rootstocks in a trial severely affected by huanglongbing.","volume":"201","author":"Bowman","year":"2016","journal-title":"Sci. Hortic."},{"key":"B8","first-page":"1049","article-title":"Total nitrogen","author":"Bremner","year":"1965","journal-title":"Methods of Soil Analysis: Part 2 1"},{"key":"B9","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1080\/14786419.2018.1561682","article-title":"Residues of 165 pesticides in citrus fruits using LC-MS\/MS: a study of the pesticides distribution from the peel to the pulp.","volume":"34","author":"Calvaruso","year":"2020","journal-title":"J. Nat. Prod. Res."},{"key":"B10","doi-asserted-by":"crossref","first-page":"C199","DOI":"10.1111\/j.1750-3841.2009.01495.x","article-title":"Chemical characterization of orange juice from trees infected with citrus greening (Huanglongbing).","volume":"75","author":"Dagulo","year":"2010","journal-title":"J. Food Sci."},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.01976","article-title":"Effect of huanglongbing or greening disease on orange juice quality, a review.","volume":"9","author":"Dala-Paula","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1016\/j.lwt.2018.01.083","article-title":"Active taste compounds in juice from oranges symptomatic for Huanglongbing (HLB) citrus greening disease.","volume":"91","author":"Dala-Paula","year":"2018","journal-title":"LWT Food Sci. Technol."},{"key":"B13","author":"Diepenbrock","year":"2019","journal-title":"2019-2020 Florida Citrus Production Guide: Pesticides Registered for Use on Florida Citrus."},{"key":"B14","doi-asserted-by":"publisher","first-page":"1451","DOI":"10.1093\/jxb\/ert035","article-title":"What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells.","volume":"64","author":"Etienne","year":"2013","journal-title":"J. Exp. Bot."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1111\/j.1365-3059.2010.02328.x","article-title":"Changes in carbohydrate metabolism in Citrus sinensis infected with \u2018Candidatus Liberibacter asiaticus\u2019.","volume":"59","author":"Fan","year":"2010","journal-title":"J. Plant Pathol."},{"key":"B16","first-page":"606","article-title":"Phosphonate fungicides for control of diseases caused by Phytophthora.","volume":"71","author":"Fenn","year":"1987","journal-title":"California Avocado Society Yearbook"},{"key":"B17","doi-asserted-by":"publisher","first-page":"2028","DOI":"10.21273\/HORTSCI15390-20","article-title":"Sweet orange orchard architecture design, fertilizer and irrigation management strategies under Huanglongbing-endemic conditions in the Indian River Citrus District.","volume":"55","author":"Ferrarezi","year":"2020","journal-title":"Hort. Science"},{"key":"B18","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.cropro.2012.01.004","article-title":"Inconsequential effect of nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress.","volume":"36","author":"Gottwald","year":"2012","journal-title":"Crop Protect."},{"key":"B19","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1653\/0015-4040(2004)087[0330:acpspa]2.0.co;2","article-title":"Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida.","volume":"87","author":"Halbert","year":"2004","journal-title":"Florida Entomol."},{"key":"B20","first-page":"36","article-title":"Influence of soil-applied fertilizer on greening development in new growth flushes of sweet orange.","volume":"12","author":"Handique","year":"2012","journal-title":"Proc. Florida State Hortic. Soc."},{"key":"B21","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1094\/phyto-05-17-0175-r","article-title":"Control of citrus Huanglongbing via trunk injection of plant defense activators and antibiotics.","volume":"108","author":"Hu","year":"2018","journal-title":"Phytopathology"},{"key":"B22","doi-asserted-by":"publisher","first-page":"3983","DOI":"10.1021\/acs.jafc.7b05866","article-title":"Metabolite profiling of Candidatus Liberibacter infection in Hamlin sweet oranges.","volume":"66","author":"Hung","year":"2018","journal-title":"J. Agric. Food Chem."},{"key":"B23","doi-asserted-by":"crossref","DOI":"10.1186\/s13568-019-0871-9","article-title":"Effect of different combinations of antibiotics on fruit quality and antioxidant defense system in Huanglongbing infected Kinnow orchards.","volume":"9","author":"Hussain","year":"2019","journal-title":"AMB Express"},{"key":"B24","doi-asserted-by":"publisher","first-page":"2370","DOI":"10.1021\/acs.jafc.7b00892","article-title":"Investigation on key molecules of Huanglongbing (HLB)-induced orange juice off-flavor.","volume":"66","author":"Kiefl","year":"2017","journal-title":"J. Agric. Food Chem."},{"key":"B25","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.mimet.2005.10.018","article-title":"Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing.","volume":"66","author":"Li","year":"2006","journal-title":"J. Microbiol.Methods"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1016\/j.infrared.2019.103138","article-title":"Non-destructive determination of soluble solids content using a multi-region combination model in hybrid citrus.","volume":"104","author":"Li","year":"2020","journal-title":"Infrared Phys. Technol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"3307","DOI":"10.1093\/jxb\/ers070","article-title":"Gene expression in Citrus sinensis fruit tissues harvested from huanglongbing-infected trees: comparison with girdled fruit.","volume":"63","author":"Liao","year":"2012","journal-title":"J. Exp.Bot."},{"key":"B28","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1002\/jsfa.7061","article-title":"Huanglongbing modifies quality components and flavonoid content of \u2018Valencia\u2019oranges.","volume":"96","author":"Massenti","year":"2016","journal-title":"J. Sci.Food Agric."},{"key":"B29","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1097\/mrm.0000000000000100","article-title":"Carvacrol and thymol: strong antimicrobial agents against resistant isolates.","volume":"28","author":"Memar","year":"2017","journal-title":"Rev. Med. Microbiol."},{"key":"B30","year":"2020","journal-title":"Florida Department of Agriculture and Consumer Services."},{"key":"B31","author":"Morgan","year":"2020","journal-title":"Nutrition of Florida Citrus Trees"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-13-59","article-title":"The effect of \u2018Candidatus Liberibacter asiaticus\u2019 infection on the proteomic profiles and nutritional status of pre-symptomatic and symptomatic grapefruit (Citrus paradisi) plants.","volume":"13","author":"Nwugo","year":"2013","journal-title":"BMC Plant Biol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.21273\/hortsci15255-20","article-title":"Ray Ruby\u2019grapefruit affected by huanglongbing II. planting density, soil, and foliar nutrient management.","volume":"55","author":"Phuyal","year":"2020","journal-title":"HortScience"},{"key":"B34","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.21273\/hortsci12002-17","article-title":"Effect of vector control and foliar nutrition on the quality of orange juice affected by Huanglongbing: sensory evaluation.","volume":"52","author":"Plotto","year":"2017","journal-title":"HortScience"},{"key":"B35","doi-asserted-by":"crossref","first-page":"S220","DOI":"10.1111\/j.1750-3841.2010.01580.x","article-title":"Effect of Liberibacter infection (Huanglongbing or \u201cGreening\u201d disease) of citrus on orange juice flavor quality by sensory evaluation.","volume":"75","author":"Plotto","year":"2010","journal-title":"J. Food Sci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1002\/ffj.1888","article-title":"Odour and flavour thresholds for key aroma components in an orange juice matrix: esters and miscellaneous compounds.","volume":"23","author":"Plotto","year":"2008","journal-title":"Flavour Fragr. J."},{"key":"B37","doi-asserted-by":"publisher","first-page":"2076","DOI":"10.1002\/jsfa.5584","article-title":"Effect of fruit load on maturity and carotenoid content of clementine (Citrus clementina Hort. ex Tan.) fruits.","volume":"92","author":"Poiroux-Gonord","year":"2012","journal-title":"J. Sci. Food Agric."},{"key":"B38","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1071\/dn08045","article-title":"Interactions between plant nutrition and symptom expression in mandarin trees infected with the disease huanglongbing.","volume":"3","author":"Pustika","year":"2008","journal-title":"Austr. Plant Di. Notes"},{"key":"B39","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1016\/j.lwt.2014.06.020","article-title":"Effect of blending Huanglongbing (HLB) disease affected orange juice with juice from healthy orange on flavor quality.","volume":"62","author":"Raithore","year":"2015","journal-title":"LWT Food Sci. Technol."},{"key":"B40","first-page":"299","article-title":"Citrus plant nutritional profile in relation to Huanglongbing prevalence in Pakistan.","volume":"48","author":"Razi","year":"2011","journal-title":"Pakistan J. Agric. Sci."},{"key":"B41","first-page":"548","article-title":"Differential response of wheat varieties to systemic fungitoxicants applied to control Ustilago tritici (Pers.) Rostr.","volume":"55","author":"Rewal","year":"1985","journal-title":"Indian J. Agric. Sci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1007\/s10658-013-0283-7","article-title":"Relation between plant nutrition, hormones, insecticide applications, bacterial endophytes, and Candidatus Liberibacter Ct values in citrus trees infected with Huanglongbing.","volume":"137","author":"Shen","year":"2013","journal-title":"Eur. J. Plant Pathol."},{"key":"B43","first-page":"181","article-title":"Identification of physical and biochemical characteristic of mandarin (Citrus reticulata) fruit infected by huanglongbing (HLB).","volume":"5","author":"Shokrollah","year":"2011","journal-title":"Austr. J. Crop Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1093\/aepp\/ppx030","article-title":"Is area-wide pest management useful? The case of citrus greening.","volume":"39","author":"Singerman","year":"2017","journal-title":"J. Appl. Econ. Perspect. Policy"},{"key":"B45","doi-asserted-by":"crossref","first-page":"4223","DOI":"10.1021\/pr300350x","article-title":"Metabolomic analysis of citrus infection by \u2018Candidatus Liberibacter\u2019 reveals insight into pathogenicity.","volume":"11","author":"Slisz","year":"2012","journal-title":"J. Proteome Res."},{"key":"B46","first-page":"169","article-title":"The role of plant nutrients in disease development with emphasis on citrus and huanglongbing.","volume":"122","author":"Spann","year":"2009","journal-title":"Proc. Fla. State Hort. Soc."},{"key":"B47","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1002\/ps.3577","article-title":"Vector control and foliar nutrition to maintain economic sustainability of bearing citrus in Florida groves affected by huanglongbing.","volume":"70","author":"Stansly","year":"2014","journal-title":"Pest Manag. Sci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"127","DOI":"10.21273\/hortsci.51.2.127","article-title":"Conventional citrus of some scion\/rootstock combinations show field tolerance under high Huanglongbing disease pressure.","volume":"51","author":"Stover","year":"2016","journal-title":"HortScience"},{"key":"B49","year":"2020","journal-title":"Foreign Agricultural Service, Citrus: World Markets and Trade."},{"key":"B50","year":"2020","journal-title":"USDA National Agricultural Statistics Service, Citrus Forecast."},{"key":"B51","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.cropro.2016.03.013","article-title":"Mitigating citrus huanglongbing via effective application of antimicrobial compounds and thermotherapy.","volume":"84","author":"Yang","year":"2016","journal-title":"J. Crop. Protect."},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0111032","article-title":"Effective antibiotics against \u2018Candidatus Liberibacter asiaticus\u2019 in HLB-affected citrus plants identified via the graft-based evaluation.","volume":"9","author":"Zhang","year":"2014","journal-title":"PLoS One"},{"key":"B53","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1094\/phyto-09-11-0265","article-title":"A graft-based chemotherapy method for screening effective molecules and rescuing huanglongbing-affected citrus plants.","volume":"102","author":"Zhang","year":"2012","journal-title":"Phytopathology"},{"key":"B54","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1094\/phyto-09-10-0262","article-title":"Chemical compounds effective against the citrus Huanglongbing bacterium \u2018Candidatus Liberibacter asiaticus\u2019 in planta.","volume":"101","author":"Zhang","year":"2011","journal-title":"Phytopathology"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.01890","article-title":"Field evaluation of integrated management for mitigating citrus huanglongbing in Florida.","volume":"9","author":"Zhang","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1093\/mp\/sst002","article-title":"Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease.","volume":"6","author":"Zhao","year":"2013","journal-title":"Mol. Plant"}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.611287\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T15:10:37Z","timestamp":1614352237000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.611287\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,22]]},"references-count":56,"alternative-id":["10.3389\/fpls.2021.611287"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2021.611287","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,22]]},"article-number":"611287"}}