A comparison of transporter gene expression in three species of Peronospora plant pathogens during host infection

Authors: Johnson, Eric; Lyon, Rebecca; ZAITLIN, DAVID - University Of Kentucky; KHAN, ABDUL - Jamia Millia Islamia University; JAIRAJPURI, MOHAMMAD - Jamia Millia Islamia University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2023
Publication Date: 6/1/2023
Citation: Johnson, E.T., Lyon, R.M., Zaitlin, D., Khan, A.B., Jairajpuri, M.A. 2023. A comparison of transporter gene expression in three species of Peronospora plant pathogens during host infection. PLOS ONE. https://doi.org/10.1371/journal.pone.0285685.
DOI: https://doi.org/10.1371/journal.pone.0285685

Interpretive Summary: Most downy mildews that infect U.S. crops only grow on a limited number of hosts, and cannot grow on nutrients prepared in the laboratory. Because of this, the basic knowledge about nutrient acquisition of downy mildews is quite limited. This study measured the expression level of downy mildew genes that are likely essential for nutrient acquisition during infection of its plant host. The downy mildew gene expression in leaves was measured at similar timepoints after inoculation of basil, spinach and tobacco leaves with infective spores. The data indicated that several of the same genes in each organism were highly expressed at similar time points, especially those genes coding for proteins that bring important metabolites inside and out of the cell mitochondria, a specialized cell structure which significantly contributes to the energy status of each pathogen cell. The identification of these highly-expressed genes contributing to nutrient acquisition in these three plant pathogens could lead to the development of future plant protection products that reduce crop losses of these commodities caused by these downy mildews.

Technical Abstract: Protein transporters move essential metabolites across membranes in all living organisms. Downy mildew causing plant pathogens are biotrophic oomycetes that transport essential nutrients from their hosts to grow. Little is known about the functions and gene expression levels of membrane transporters produced by downy mildew causing pathogens during infection of their hosts. Approximately 170–190 nonredundant transporter genes were identified in the genomes of Peronospora belbahrii, Peronospora effusa, and Peronospora tabacina, which are specialized pathogens of basil, spinach, and tobacco, respectively. The largest groups of transporter genes in each species belonged to the major facilitator superfamily, mitochondrial carriers (MC), and the drug/metabolite transporter group. Gene expression of putative Peronospora transporters was measured using RNA sequencing data at two time points following inoculation onto leaves of their hosts. There were 16 transporter genes, seven of which were MCs, expressed in each Peronospora species that were among the top 45 most highly expressed transporter genes 5–7 days after inoculation. Gene transcripts encoding the ADP/ATP translocase and the mitochondrial phosphate carrier protein were the most abundant mRNAs detected in each Peronospora species. This study found a number of Peronospora genes that are likely critical for pathogenesis and which might serve as future targets for control of these devastating plant pathogens.