Progress on molecular genetics and manipulation of rust fungi

Authors: BAKKEREN, GUUS - Agriculture And Agri-Food Canada; Szabo, Les

Submitted to: Phytopathology
Publication Type: Literature Review
Publication Acceptance Date: 11/27/2019
Publication Date: 1/16/2020
Citation: Bakkeren, G., Szabo, L.J. 2020. Progress on molecular genetics and manipulation of rust fungi. Phytopathology. 110:532-543. https://doi.org/10.1094/PHYTO-07-19-0228-IA.
DOI: https://doi.org/10.1094/PHYTO-07-19-0228-IA

Interpretive Summary: Rust fungi are one of the largest groups of plant pathogenic fungi and cause disease across the plant kingdom including important agricultural, horticultural and forest crops. The obligate biotrophic nature of rust fungi has made studying them on a molecular genetic and biochemical level challenging. While molecular genetic work on many plant pathogens flourished, comparable research on rusts has been hampered by the inability to grow most rust fungi outside of their hosts and related to that, to develop a genetic transformation system. However, the genomics revolution has been particularly beneficial for obligate fungal pathogens, allowing at least structural gene analyses, which, coupled with transcriptomic and proteomic work, eased the way for performing molecular genetic studies using related heterologous systems. Since the "genomics revolution", many laboratories have embarked on rust fungal research. Here, we review some of the historic research, the current state of our ability to genetically manipulate rust fungi or use workarounds to assess rust gene function, and how this impacts rust disease control and agriculture, limiting ourselves to a few well-developed and important pathosystems.

Technical Abstract: Among the thousands of rust species described, many are known for their devastating effects on their hosts which include major agriculture crops and trees. Hence, for over a century, these basidiomycete pathogenic fungi have been researched and experimented with. However, due to their biotrophic nature, they are challenging organisms to work with and, needing their hosts for propagation, represent pathosystems that are not easily experimentally accessible. Indeed, efforts to perform genetics have been few and far apart for the rust fungi, though one performed in the 1950s was famously instrumental in formulating the gene-for-gene hypothesis describing pathogen-host interactions. By taking full advantage of the molecular genetic tools developed in the 1980s, research on many plant pathogenic microbes thrived, yet similar work on the rusts remained very challenging though not without some successes. However, the genomics era brought real breakthrough research for the biotrophic fungi and with innovative experimentation and the use of heterologous systems, molecular genetic analyses over the last two decades have significantly advanced our insight into the function of many rust fungus genes and their role in the interaction with their hosts. This has allowed optimizing efforts for resistance breeding and the design and testing of various novel strategies to reduce the devastating diseases they cause.