Transcriptomic analysis reveals root metabolic alteration and induction of huanglongbing resistance by sulphonamide antibiotics in huanglongbing‐affected citrus plants

Huanglongbing (HLB) is a devastating disease that affects the entire citrus plant, including the root system. Previous studies have shown that sulphonamide antibiotics can suppress titres of the pathogen that causes HLB, ‘Candidatus Liberibacter asiaticus’ (CLas), and affect root morphology in the plant through unknown mechanisms. To better understand the response of CLas‐infected roots to sulphonamide antibiotics, hydroponic cultures of CLas‐infected citrus roots were treated with sulfadimethoxine sodium (SDX), indole butyric acid (IBA), or water for 60 days to evaluate root metabolism and resistance against CLas via transcriptomic analysis. This study indicated that SDX and IBA treatments increased active root surface area in HLB‐affected citrus, which may be due to root hair and lateral root growth. CLas titres in HLB‐affected citrus roots treated with SDX were lower than those of IBA and control treatments. Function categorization indicated that plant hormone signal transduction and plant–pathogen interaction were the most markedly enriched pathways in the HLB‐affected citrus root after SDX treatment. The expression of genes involved in biosynthesis of auxin and ethylene, which are related to root hair and lateral root growth, were up‐regulated by SDX. Moreover, SDX also induced genes related to the metabolism of jasmonates, brassinosteroids, reactive oxygen species, and secondary metabolites, which are beneficial for resistance against HLB. In conclusion, we propose a model for SDX in regulating metabolic pathways in the root and resistance against CLas in HLB‐affected citrus root, which is beneficial for recovering an HLB‐affected citrus root system and combating CLas.

[1]  M. Ochagavía,et al.  ‘Candidatus Liberibacter asiaticus’, Causal Agent of Citrus Huanglongbing, Is Reduced by Treatment with Brassinosteroids , 2016, PloS one.

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

[3]  Hao Cheng,et al.  Transcriptome Analysis of Indole-3-Butyric Acid-Induced Adventitious Root Formation in Nodal Cuttings of Camellia sinensis (L.) , 2014, PloS one.

[4]  Thomas H. Spreen,et al.  An Economic Assessment of the Impact of Huanglongbing on Citrus Tree Plantings in Florida , 2014 .

[5]  M. Sussman,et al.  SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis[C][W] , 2014, Plant Cell.

[6]  J. Graham,et al.  Association of ‘Candidatus Liberibacter asiaticus’ root infection, but not phloem plugging with root loss on huanglongbing-affected trees prior to appearance of foliar symptoms , 2014 .

[7]  F. Capolongo,et al.  Accumulation and Response of Willow Plants Exposed to Environmental Relevant Sulfonamide Concentrations , 2014, International journal of phytoremediation.

[8]  I. Szarejko,et al.  Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. , 2013, Journal of plant physiology.

[9]  Niranjan Nagarajan,et al.  The draft genome of sweet orange (Citrus sinensis) , 2012, Nature Genetics.

[10]  K. Shirasu,et al.  Sulfonamides identified as plant immune-priming compounds in high-throughput chemical screening increase disease resistance in Arabidopsis thaliana , 2012, Front. Plant Sci..

[11]  D. Lin,et al.  Transcriptome Profiling of Citrus Fruit Response to Huanglongbing Disease , 2012, PloS one.

[12]  D. Scheel,et al.  Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. , 2011, The Plant journal : for cell and molecular biology.

[13]  R. Verpoorte,et al.  Chalcone synthase and its functions in plant resistance , 2011, Phytochemistry Reviews.

[14]  H. Doddapaneni,et al.  Complete genome sequence of citrus huanglongbing bacterium, 'Candidatus Liberibacter asiaticus' obtained through metagenomics. , 2009, Molecular plant-microbe interactions : MPMI.

[15]  Y. Guisez,et al.  Different stresses, similar morphogenic responses: integrating a plethora of pathways. , 2009, Plant, cell & environment.

[16]  Ho Bang Kim,et al.  Ricebending lamina 2 (bla2) mutants are defective in a cytochrome P450 (CYP734A6) gene predicted to mediate brassinosteroid catabofism , 2006, Journal of Plant Biology.

[17]  Richard A Brain,et al.  Herbicidal effects of sulfamethoxazole in Lemna gibba: using p-aminobenzoic acid as a biomarker of effect. , 2008, Environmental science & technology.

[18]  H. Song,et al.  A Role for a Menthone Reductase in Resistance against Microbial Pathogens in Plants1[C][W][OA] , 2008, Plant Physiology.

[19]  Maido Remm,et al.  Enhancements and modifications of primer design program Primer3 , 2007, Bioinform..

[20]  Thomas A. Obreza,et al.  Orange Tree Fibrous Root Length Distribution in Space and Time , 2007 .

[21]  W. Finch-Savage,et al.  Seed dormancy and the control of germination. , 2006, The New phytologist.

[22]  Wenbin Li,et al.  Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. , 2006, Journal of microbiological methods.

[23]  Changhua Zhu,et al.  Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis. , 2006, Journal of experimental botany.

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

[25]  Mu Zx,et al.  Hydraulic conductivity of whole root system is better than hydraulic conductivity of single root in correlation with the leaf water status of maize , 2006 .

[26]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[27]  B. Bartel,et al.  Auxin: regulation, action, and interaction. , 2005, Annals of botany.

[28]  M. Yano,et al.  A Novel Cytochrome P450 Is Implicated in Brassinosteroid Biosynthesis via the Characterization of a Rice Dwarf Mutant, dwarf11, with Reduced Seed Length , 2005, The Plant Cell Online.

[29]  A. Hetherington,et al.  The generation of Ca(2+) signals in plants. , 2004, Annual review of plant biology.

[30]  J. Ecker,et al.  Type-A Arabidopsis Response Regulators Are Partially Redundant Negative Regulators of Cytokinin Signaling Online version contains Web-only data. , 2004, The Plant Cell Online.

[31]  G. Hagen,et al.  Auxin-responsive gene expression: genes, promoters and regulatory factors , 2002, Plant Molecular Biology.

[32]  M. Böttger Apical dominance in roots of Pisum sativum L. , 2004, Planta.

[33]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[34]  N. Goto,et al.  Auxin and Ethylene Response Interactions during Arabidopsis Root Hair Development Dissected by Auxin Influx Modulators , 2002, Plant Physiology.

[35]  P. B. Tinker,et al.  Solute Movement in the Rhizosphere , 2000 .

[36]  G. Prestwich,et al.  ENZYMATIC CYCLIZATION OF SQUALENE AND OXIDOSQUALENE TO STEROLS AND TRITERPENES , 1993 .