Spray‐induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake

• Published in: Plant biotechnology journal Vol. 19; no. 9; pp. 1756 - 1768
• Main Authors: Qiao, Lulu, Lan, Chi, Capriotti, Luca, Ah‐Fong, Audrey, Nino Sanchez, Jonatan, Hamby, Rachael, Heller, Jens, Zhao, Hongwei, Glass, N. Louise, Judelson, Howard S., Mezzetti, Bruno, Niu, Dongdong, Jin, Hailing
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.09.2021; Society for Experimental Biology; Association of Applied Biology; John Wiley and Sons Inc
• Subjects: Agricultural production; Aspergillus niger; BASIC BIOLOGICAL SCIENCES; biotechnology; Botrytis cinerea; Crop diseases; Crops; Developmental stages; Disease control; Disease management; Double-stranded RNA; Efficiency; Flowers & plants; Fungi; Gene silencing; Genes; Genetic engineering; Glomerella cingulata; Health aspects; Leaves; Medical research; Medicine, Experimental; Microorganisms; Microscopy; Pathogens; Phytophthora infestans; Plant diseases; plant pathogens; Ribonucleic acid; RNA; RNA interference; RNA-mediated interference; Sclerotinia sclerotiorum; Signs and symptoms; small RNA; species; spray-induced gene silencing; Thanatephorus cucumeris; Topical application; Trichoderma virens; uptake efficiency; Verticillium dahliae; Virulence; Virulence (Microbiology); RNA interference; uptake efficiency; double-stranded RNA; small RNA; spray-induced gene silencing
• ISSN: 1467-7644; 1467-7652; 1467-7652
• DOI: 10.1111/pbi.13589

Summary Recent discoveries show that fungi can take up environmental RNA, which can then silence fungal genes through environmental RNA interference. This discovery prompted the development of Spray‐Induced Gene Silencing (SIGS) for plant disease management. In this study, we aimed to determine the efficacy of SIGS across a variety of eukaryotic microbes. We first examined the efficiency of RNA uptake in multiple pathogenic and non‐pathogenic fungi, and an oomycete pathogen. We observed efficient double‐stranded RNA (dsRNA) uptake in the fungal plant pathogens Botrytis cinerea, Sclerotinia sclerotiorum, Rhizoctonia solani, Aspergillus niger and Verticillium dahliae, but no uptake in Colletotrichum gloeosporioides, and weak uptake in a beneficial fungus, Trichoderma virens. For the oomycete plant pathogen, Phytophthora infestans, RNA uptake was limited and varied across different cell types and developmental stages. Topical application of dsRNA targeting virulence‐related genes in pathogens with high RNA uptake efficiency significantly inhibited plant disease symptoms, whereas the application of dsRNA in pathogens with low RNA uptake efficiency did not suppress infection. Our results have revealed that dsRNA uptake efficiencies vary across eukaryotic microbe species and cell types. The success of SIGS for plant disease management can largely be determined by the pathogen’s RNA uptake efficiency.