Cooper, William Rodney

Abstract Bactericera maculipennis (Crawford) and Bactericera cockerelli (Šulc) (Hemiptera: Triozidae) share hosts within the Solanaceae and Convolvulaceae (Solanales), and both are associated with “Candidatus Liberibacter solanacearum” (Lso). Lso, transmitted by B. cockerelli, causes diseases in solanaceous crops including zebra chip disease of potato. Up to 50% of B. maculipennis adults also harbor Lso, but transmission of Lso to plants by this psyllid has not been confirmed yet. The only documented field host of B. maculipennis in the Pacific Northwest is Convolvulus arvensis L. (Convolvulaceae) but diagnostic methods fail to detect Lso in leaves of this plant. It is therefore unclear how Lso persists within B. maculipennis populations. We surveyed species of Convolvulaceae and Solanaceae for B. maculipennis and report a widespread association between B. maculipennis and Lso throughout the western United States. Diagnostic polymerase chain reaction failed to detect Lso from leaves of C. arvensis yet readily detected Lso from stems where B. maculipennis nymphs tend to feed. Bactericera maculipennis transmitted Lso to species of Convolvulaceae in greenhouse experiments, confirming vector competency. We report high rates of Lso infection in populations of both B. maculipennis and B. cockerelli occurring on C. arvensis, but occurrence of B. cockerelli on C. arvensis was limited to autumn months only and with very low populations. Results suggest C. arvensis is a non-crop reservoir of Lso but do not suggest that B. maculipennis is a direct threat to solanaceous crops or that C. arvensis is a major source of Lso-infected B. cockerelli colonizing potato fields.

IntroductionCandidatus 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 pathogenic 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.MethodsNext-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.ResultsPlants infected with CLso haplotype B saw 229 genes upregulated when compared to uninfected plants, while 1,135 were downregulated. Healthy tomato plants and plants infected by haplotype A had similar expression levels, which is 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 downregulated 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.DiscussionThis study provides insights into plants’ defense and functional decline due to pathogenic CLso using whole transcriptome sequencing and qPCR validation. Our results show 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.

The potato/tomato psyllid, Bactericera cockerelli (Šulc), is among the most important pests of solanaceous crops as a vector of the pathogen ‘Candidatus Liberibacter solanacearum’ (Lso). Lso-infected psyllids often arrive in crop fields from various wild species of Solanaceae and Convolvulaceae, especially those that provide early-season hosts for the vector. Physalis species are perennial plants within the family Solanaceae with often broad geographical distributions that overlap those of B. cockerelli, yet the status of many Physalis species as hosts for B. cockerelli or Lso remains unknown. Our objective was to determine whether wild Physalis species that occur in the potato-growing region of Galeana, Nuevo León, Mexico, host B. cockerelli populations and whether they also are susceptible to Lso. Sampling was carried out in the potato-growing zone of Galeana, Nuevo León, Mexico, where unidentified Physalis spp. are common. In March to October 2021, a wild plant identified as Physalis virginiana was observed; eggs, nymphs, and adults of B. cockerelli were observed on these plants throughout the growing season, and nymphs completed development on these plants under laboratory conditions. Lso also was detected in 22 of the 93 (23.7%) wild P. virginiana plants using conventional PCR, while 13.3% of B. cockerelli adults that emerged from P. virginiana cuttings harbored the pathogen. This is the first report that P. virginiana is a host for B. cockerelli and for Lso. These results suggest that P. virginiana is a likely source of Lso-infected psyllids colonizing solanaceous crops in northeastern Mexico. The importance of P. virginiana and other wild hosts on the population dynamics of the vector and pathogen should be investigated to assist in pest management decision-making.