The functional decline of tomato plants infected by Candidatus Liberibacter solanacearum: an RNA-Seq transcriptomic analysis

Authors: CHUAN, JIACHENG - University Of Prince Edward Island; NIE, JINGBAI - Canadian Food Inspection Agency; Cooper, William - Rodney; CHEN, WEN - University Of Prince Edward Island; HALE, LAWRENCE - University Of Prince Edward Island; LE, SEAN - Canadian Food Inspection Agency

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2024
Publication Date: 2/1/2024
Citation: Chuan, J., Nie, J., Cooper, W.R., Chen, W., Hale, L., Le, S. 2024. The functional decline of tomato plants infected by Candidatus Liberibacter solanacearum: an RNA-Seq transcriptomic analysis. Frontiers in Plant Science. 15:1325254. https://doi.org/10.3389/fpls.2024.1325254.
DOI: https://doi.org/10.3389/fpls.2024.1325254

Interpretive Summary: Candidatus Liberibacter solanacearum (CLso) is an insect-vectored pathogen of tomato and potato responsible for over $1 billion worldwide in management costs and yield losses. Currently, the only means to reduce diseases caused by cLso is the extensive use of insecticides to reduce populations of insect vectors. The development of crop cultivars that are resistant to cLso would provide growers with a means to control diseases caused by cLso without the use of insecticides. A major challenge in the development of resistant varieties is the occurrence of multiple strains of cLso bacteria that cause different levels of disease symptoms in crops. Researchers at the USDA-ARS in Wapato, WA collaborated with a team from University of Prince Edward Island and the Canadian Food Inspection Service to characterize the underlying molecular mechanisms for plant disease caused by various cLso haplotypes in tomato by analyzing changes in gene expression in infected and uninfected plants. They found that disease symptoms were associated with increased consumption of carbohydrates, and reduced cell membrane fluidity, cell signaling, and plant defense. Overall, the results will help research teams target specific molecular pathways to develop crops that are resistant to cLso, and in doing so provide growers with cost-effective and environmentally friendly means of disease management.

Technical Abstract: Candidatus Liberibacter solanacearum (CLso) is a regulated plant pathogen in European and some Asian countries, associated with severe diseases in economically important Apiaceous and Solanaceous crops, including potato, tomato, and carrot. Eleven haplotypes of CLso have been identified based on the difference in rRNA and conserved genes and host and pathogenicity. Although it is pathologic to a wide range of plants, the mechanisms of plant response and functional decline of host plants are not well defined. This study aims to describe the underlying mechanism of the functional decline of tomato plants infected by CLso by analyzing the transcriptomic response of tomato plants to CLso haplotypes A and B. Next-generation sequencing (NGS) data were generated from total RNA of tomato plants infected by CLso haplotypes A and B, and uninfected tomato plants, while qPCR analysis was used to validate the in-silico expression analysis. Gene Ontology and KEGG pathways were enriched using differentially expressed genes. Plants infected with cLso haplotype B had 229 genes were upregulated and 1135 were downregulated compared to uninfected plants. Healthy tomato plants and plants infected by haplotype A had similar expression levels, consistent with the fact that CLso haplotype A does not show apparent symptoms in tomato plants. Photosynthesis and starch biosynthesis were impaired while starch amylolysis was promoted in plants infected by cLso haplotype B compared with uninfected plants. The changes in pathway gene expression suggest that carbohydrate consumption in infected plants was more extensive than accumulation. In addition, cell-wall-related genes, including steroid biosynthesis pathways, were down regulated in plants infected with cLso haplotype B suggesting a reduction in membrane fluidity, cell signaling, and defense against bacteria. In addition, genes in phenylpropanoid metabolism and DNA replication were generally suppressed by cLso infection, affecting plant growth and defense. This study provides insights into plants’ defense and functional decline to pathogenic CLso, using whole transcriptome sequencing and qPCR validation. Our results showed how tomato plants react in metabolic pathways during the deterioration caused by pathogenic CLso. Understanding the underlying mechanisms can enhance disease control and create opportunities for breeding resistant or tolerant varieties.