Transcriptomic analysis reveals root metabolic alteration and induction of Huanglongbing resistance by Sulfonamide antibiotics in Huanglongbing-affected citrus plants

Authors: YANG, CHUANYU - University Of Florida; HUANG, J - Guangxi University; POWELL, CHARLES - University Of Florida; Duan, Ping; ANCONA, VERONICA - Texas A&M University; ZHANG, MUQING - University Of Florida

Submitted to: Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/29/2020
Publication Date: 1/29/2020
Citation: Yang, C., Huang, J.Y., Powell, C., Duan, Y., Ancona, V., Zhang, M. 2020. Transcriptomic analysis reveals root metabolic alteration and induction of Huanglongbing resistance by Sulfonamide antibiotics in Huanglongbing-affected citrus plants. Plant Pathology. https://doi.org/10.1111/ppa.13154.
DOI: https://doi.org/10.1111/ppa.13154

Interpretive Summary: Citrus huanglongbing (HLB) is currently the most devastating citrus disease and has caused enormous economic losses to many citrus growing regions of the world. One of the devastating effects caused by HLB is the loss and degeneration of citrus roots, which result in yield reduction and eventually tree death. Our previous studies demonstrated sulfonamide antibiotics can suppress the HLB pathogen titers and induce root hair and lateral root growth in citrus plants . In this study, we conduct transcriptomic and metagenomic analyses to reveal the mechanisms underlying the root morphology alteration and resistance against Candidatus Liberibacter asiaticus (CLas) in HLB-affected citrus in response to sulfonamide antibiotics.

Technical Abstract: Huanglongbing (HLB) is a devastating systemic disease that affects the entire citrus plant including the root system. Previous studies have shown that sulfonamide antibiotics can suppress the causing pathogen Candidatus Liberibacter asiaticus (CLas) titers and induce root hair and lateral root growth in several plants through unknown mechanisms. To better understand the response of CLas-infected roots to sulfonamide antibiotics, hydroponic cultures of CLas-infected citrus roots were treated with sulfadimethoxine sodium (SDX, 10 ppm), indole butyric acid (IBA, 10 ppm), or water (CK) for 60 days to evaluate root morphology and conduct transcriptomic and metagenomic analyses. Results indicated that SDX and IBA treatments increased active root surface area in HLB-affected citrus. CLas titers in HLB-affected citrus roots treated with SDX were lower than those of IBA and CK treatments. In HLB-affected citrus, SDX treatment induced the expression of genes including tryptophan synthase beta chain 2, glutamyl-tRNA(Gln) amidotransferase subunit A, and glutathione S-transferase genes, which are involved in the metabolism of plant hormones and the regulation of root hair and lateral growth. SDX also induced genes (MCY4, cytochrome P450 (CYP724B1), cyclic nucleotide-gated ion channel, and neomenthol dehydrogenase genes) related to the metabolism of jasmonates, brassinosteroids, reactive oxygen species, and secondary metabolites, which are beneficial for resistance against HLB. Additionally, some special Operational Taxonomic Units (OTUs) from the Sphingomonadaceae family, Burkholderiales order, and Desulfococcus genus, which are involved in increased resistance to plant pathogens, were more abundant in SDX treatments. Several special OTUs belonging to the Devosia, Achromobacter, Pseudomonas, and Bacillus genus, which are associated in regulating root hair and lateral root growth, were also enriched by SDX. This study reveals the mechanisms underlying the root morphology alteration and resistance against CLas in HLB-affected citrus in response to sulfonamide antibiotics.