Control of Citrus Huanglongbing via Trunk Injection of Plant Defense Activators and Antibiotics.

Citrus huanglongbing (HLB) or greening is a devastating disease of citrus worldwide and no effective control measure is currently available. Plant defense activators environmentally friendly compounds capable of inducing resistance against many plant pathogens. Earlier studies showed that foliar spray of plant defense inducers could slow down HLB disease progress. In this study, eight plant defense activators and three antibiotics were evaluated in three field trials for their effect to control HLB by trunk injection of young and mature sweet orange trees. Results showed that four trunk injections of several activators, including salicylic acid, oxalic acid, acibenzolar-S-methyl, and potassium phosphate, provided significant control of HLB by suppressing 'Candidatus Liberibacter asiaticus' titer and disease progress. Trunk injection of penicillin, streptomycin, and oxytetracycline hydrochloride resulted in excellent control of HLB. In general, antibiotics were more effective in reduction of 'Ca. L. asiaticus' titer and HLB symptom expressions than plant defense activators. These treatments also resulted in increased yield and better fruit quality. Injection of both salicylic acid and acibenzolar-S-methyl led to significant induction of pathogenesis-related (PR) genes PR-1 and PR-2 genes. Meanwhile, injection of either potassium phosphate or oxalic acid resulted in significant induction of PR-2 or PR-15 gene expression, respectively. These results suggested that HLB diseased trees remained inducible for systemic acquired resistance under field conditions. In summary, this study presents information regarding controlling HLB via trunk injection of plant defense activators and antibiotics, which helps citrus growers in decision making regarding developing an effective HLB management program.

[1]  Tony Jenkins,et al.  A First Look , 2004 .

[2]  S. Halbert,et al.  ASIAN CITRUS PSYLLIDS (STERNORRHYNCHA: PSYLLIDAE) AND GREENING DISEASE OF CITRUS: A LITERATURE REVIEW AND ASSESSMENT OF RISK IN FLORIDA , 2004 .

[3]  P. Trivedi,et al.  Field Evaluation of Plant Defense Inducers for the Control of Citrus Huanglongbing. , 2016, Phytopathology.

[4]  H. Piepho,et al.  The area under the disease progress stairs: calculation, advantage, and application. , 2012, Phytopathology.

[5]  L. Korsten,et al.  Citrus Huanglongbing: Review, Present status and Future Strategies , 2004 .

[6]  W. Dixon,et al.  Heat treatment eliminates 'Candidatus Liberibacter asiaticus' from infected citrus trees under controlled conditions. , 2013, Phytopathology.

[7]  F. Obanor,et al.  Efficacy of systemic acquired resistance inducers in olive leaf spot management , 2012, Australasian Plant Pathology.

[8]  Piękna-Grochala Justyna,et al.  Induction of resistance against pathogens by β-aminobutyric acid , 2013, Acta Physiologiae Plantarum.

[9]  A. Berna,et al.  Germins and germin-like proteins: Plant do-all proteins. But what do they do exactly? , 2001 .

[10]  S. Leite,et al.  Salicylic acid degradation from aqueous solutions using Pseudomonas fluorescens HK44: parameters studies and application tools , 2007 .

[11]  J. Graham,et al.  Soil Application of SAR Inducers Imidacloprid, Thiamethoxam, and Acibenzolar-S-Methyl for Citrus Canker Control in Young Grapefruit Trees. , 2011, Plant disease.

[12]  J. Graham,et al.  Lack of Control of Citrus Canker by Induced Systemic Resistance Compounds. , 2004, Plant disease.

[13]  J. Grosser,et al.  Transgenic Citrus Expressing an Arabidopsis NPR1 Gene Exhibit Enhanced Resistance against Huanglongbing (HLB; Citrus Greening) , 2015, PloS one.

[14]  C. Richard,et al.  Photochemical transformation of the plant activator Acibenzolar-S-methyl in solution , 2017 .

[15]  J. Burns,et al.  Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker , 2009, European Journal of Plant Pathology.

[16]  Alan L. Jones,et al.  Effect of Treating Apple Trees with Acibenzolar-S-Methyl on Fire Blight and Expression of Pathogenesis-Related Protein Genes. , 2002, Plant disease.

[17]  R. M. Goodman,et al.  Systemic acquired resistance and induced systemic resistance in conventional agriculture , 2004 .

[18]  J. Bloomquist,et al.  Chemical control of the Asian citrus psyllid and of huanglongbing disease in citrus. , 2015, Pest management science.

[19]  W. Kaiser,et al.  Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? , 2000 .

[20]  S. Aćimović,et al.  Control of fire blight (Erwinia amylovora) on apple trees with trunk-injected plant resistance inducers and antibiotics and assessment of induction of pathogenesis-related protein genes , 2015, Front. Plant Sci..

[21]  B. Duffy,et al.  Use of antibiotics in plant agriculture. , 2012, Revue scientifique et technique.

[22]  P. Nový,et al.  In vitro synergistic effects of baicalin with oxytetracycline and tetracycline against Staphylococcus aureus. , 2011, The Journal of antimicrobial chemotherapy.

[23]  Shouan Zhang,et al.  Evaluation of systemic acquired resistance inducers for control of downy mildew on basil , 2012 .

[24]  U. Sagaram,et al.  Quantification of viable Candidatus Liberibacter asiaticus in hosts using quantitative PCR with the aid of ethidium monoazide (EMA) , 2009, European Journal of Plant Pathology.

[25]  M. Doud,et al.  Effective Antibiotics against ‘Candidatus Liberibacter asiaticus’ in HLB-Affected Citrus Plants Identified via the Graft-Based Evaluation , 2014, PloS one.

[26]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[27]  Kenneth B. Johnson,et al.  INTEGRATED CONTROL OF FIRE BLIGHT WITH ANTAGONISTS AND OXYTETRACYCLINE , 2008 .

[28]  N. Havis,et al.  Controlling crop diseases using induced resistance: challenges for the future. , 2013, Journal of experimental botany.

[29]  L. Gardan,et al.  PERSISTENCE OF STREPTOMYCIN IN PEAR AND APPLE TREES , 1984 .

[30]  R. Ferreira,et al.  The role of plant defence proteins in fungal pathogenesis. , 2007, Molecular plant pathology.

[31]  J. Bové,et al.  Huanglongbing: a destructive, newly-emerging, century-old disease of citrus [Asia; South Africa; Brazil; Florida] , 2006 .

[32]  K. Sabet THE EFFECTS OF STREPTOMYCIN AND TERRAMYCIN, SINGLY AND IN COMBINATION, ON THE LEAF BLIGHT DISEASE OF MAIZE CAUSED BY BACTERIUM CAROTOVORUUM F. ZEAE SABET , 1956 .

[33]  M. Richardson,et al.  SYNERGISTIC ACTION OF STREPTOMYCIN WITH OTHER ANTIBIOTICS ON INTRACELLULAR BRUCELLA ABORTUS IN VITRO , 1962, Journal of bacteriology.

[34]  D. Walters,et al.  Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions , 2009, The Journal of Agricultural Science.

[35]  F. Roka,et al.  Vector control and foliar nutrition to maintain economic sustainability of bearing citrus in Florida groves affected by huanglongbing. , 2014, Pest management science.

[36]  E. Ward,et al.  Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Jiahuai Hu,et al.  Evaluation of the Spatiotemporal Dynamics of Oxytetracycline and Its Control Effect Against Citrus Huanglongbing via Trunk Injection. , 2016, Phytopathology.

[38]  M. Daugherty,et al.  Temporal progression of 'Candidatus Liberibacter asiaticus' infection in citrus and acquisition efficiency by Diaphorina citri. , 2014, Phytopathology.

[39]  V. Flors,et al.  Preventive and post‐infection control of Botrytis cinerea in tomato plants by hexanoic acid , 2008 .

[40]  Tim R. Gottwald,et al.  Citrus Huanglongbing: the pathogen and its impact. , 2007 .

[41]  J. Bergelson,et al.  Costs of induced responses in plants , 2003 .

[42]  L. W. Timmer,et al.  Greenhouse Evaluation of Products That Induce Host Resistance for Control of Scab, Melanose, and Alternaria Brown Spot of Citrus. , 2003, Plant disease.

[43]  T. Gottwald,et al.  Inconsequential effect of nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress , 2012 .

[44]  T. Boller,et al.  Antifungal Hydrolases in Pea Tissue : II. Inhibition of Fungal Growth by Combinations of Chitinase and beta-1,3-Glucanase. , 1988, Plant physiology.

[45]  M. Maraschin,et al.  Antifungal activity of salicylic acid against Penicillium expansum and its possible mechanisms of action. , 2015, International journal of food microbiology.

[46]  L. Pérez,et al.  Efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance against tobacco blue mould caused by Peronospora hyoscyami f. sp. tabacina , 2003 .

[47]  Yuxian Xia,et al.  Development and application of molecular-based diagnosis for ' Candidatus Liberibacter asiaticus', the causal pathogen of citrus huanglongbing , 2006 .

[48]  K. Mendgen,et al.  PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. , 1999, The Plant journal : for cell and molecular biology.

[49]  P. Aranega-Bou,et al.  Priming of plant resistance by natural compounds. Hexanoic acid as a model , 2014, Front. Plant Sci..

[50]  P. Trivedi,et al.  'Candidatus Liberibacter asiaticus' Encodes a Functional Salicylic Acid (SA) Hydroxylase That Degrades SA to Suppress Plant Defenses. , 2017, Molecular plant-microbe interactions : MPMI.