4.7 Article

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

Journal

PLANT BIOTECHNOLOGY JOURNAL
Volume 19, Issue 9, Pages 1756-1768

Publisher

WILEY
DOI: 10.1111/pbi.13589

Keywords

spray‐ induced gene silencing; small RNA; RNA interference; double‐ stranded RNA; uptake efficiency

Funding

  1. National Institute of Health [R01 GM093008, R35 GM136379-01]
  2. National Science Foundation [IOS-1557812, IOS-2017314, DBI-1922642]
  3. United States Department of Agriculture National Institute of Food and Agriculture [2021-67013-34258]
  4. Australian Research Council Industrial Transformation Research Hub [IH190100022]
  5. CIFAR `Fungal Kingdom' fellowship
  6. Jiangsu Agricultural Science and Technology Innovation Fund of China [CX(19)3103]
  7. U.S. Department of Energy, Office of Science, Office of Biological & Environmental Research [DE-AC02-05CH11231]
  8. Australian Research Council [IH190100022] Funding Source: Australian Research Council

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Recent discoveries show that fungi can uptake environmental RNA to silence fungal genes through RNA interference, leading to the development of Spray-Induced Gene Silencing (SIGS) for plant disease management. The efficiency of RNA uptake varies across eukaryotic microbe species and cell types, which plays a critical role in determining the success of SIGS for plant disease management.
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.

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