Advances in understanding obligate biotrophy in rust fungi

Abstract

Summary Rust fungi (Pucciniales) are the largest group of plant pathogens and represent one of the most devastating threats to agricultural crops worldwide. Despite the economic importance of these highly specialized pathogens, many aspects of their biology remain obscure, largely because rust fungi are obligate biotrophs. The rise of genomics and advances in high‐throughput sequencing technology have presented new options for identifying candidate effector genes involved in pathogenicity mechanisms of rust fungi. Transcriptome analysis and integrated bioinformatics tools have led to the identification of key genetic determinants of host susceptibility to infection by rusts. Thousands of genes encoding secreted proteins highly expressed during host infection have been reported for different rust species, which represents significant potential towards understanding rust effector function. Recent high‐throughput in planta expression screen approaches (effectoromics) have pushed the field ahead even further towards predicting high‐priority effectors and identifying avirulence genes. These new insights into rust effector biology promise to inform future research and spur the development of effective and sustainable strategies for managing rust diseases.

Plants make galls to accommodate foreigners: some are friends, most are foes

“…New stem rust strains arising on the alternate host barberry are sometimes able to overcome Resistance genes deployed in wheat (Zhao et al , ). Fortunately, hundreds of Resistance genes have been discovered in wheat and its relatives, among which have been found genes effective against new stem rust strains (Singh et al , ; Dean et al , ; Harris et al , ; Lorrain et al , ). This is also the case for the Hessian fly, Mayetiola destructor , an insect pest of wheat that caused havoc when it invaded North America in the late eighteenth century (Harris et al , ).…”

“…Genome sequencing of antagonists of plants predicts ‘effector candidates’ based on screening of in silico ‐translated products for presence of an N‐terminal signal peptide, protein size, and homology to known sequences (Sperschneider et al , ; Thordal‐Christensen et al , ). Predictions of which effector candidates are most important for colonization – as well as which effectors are encoded by parasite Avirulence genes – are being refined by ‘effectoromics’, which involves high‐throughput in planta expression screen approaches (Lorrain et al , ). Fungal rust species – among which are many gall‐inducing species – are noteworthy for having thousands of genes that encode secreted proteins that are strongly expressed during colonization (Lorrain et al , ).…”

“…Predictions of which effector candidates are most important for colonization – as well as which effectors are encoded by parasite Avirulence genes – are being refined by ‘effectoromics’, which involves high‐throughput in planta expression screen approaches (Lorrain et al , ). Fungal rust species – among which are many gall‐inducing species – are noteworthy for having thousands of genes that encode secreted proteins that are strongly expressed during colonization (Lorrain et al , ). The genome of the Hessian fly, a member of a large gall‐inducing insect clade, predicted 1400 effector candidates (Zhao et al , ).…”

“…A genomic 'signature' of the arms race in plants is the expansion of gene families encoding traits that play a role in their most important biotic interactions (Meyers et al, 2003;Harris et al, 2014;Plomian et al, 2018;Hipp et al, 2019). Likewise, the genomic 'signature' of the arms race in parasites is expansion of gene families encoding traits that enable colonization and maximal exploitation of the plant (Zhao et al, 2015;Lorrain et al, 2019).…”

Transcriptome analysis of apple leaves infected by the rust fungus Gymnosporangium yamadae at two sporulation stages (spermogonia and aecia) reveals specific host responses, rust pathogenesis-related genes and a shift in the phyllosphere fungal community composition

“…239 These molecular determinants are conserved across rust species and may play an 240 important role in pathogenesis-related processes. 241 242 Prediction of in planta secreted proteins expressed by G. yamadae during apple leaf 243 infection 244 Rust fungi possess very large repertoires of secreted proteins (SPs) that contain effectors, 245 which have significant roles in the establishment of compatible interactions with their host 246 plants (Lorrain et al 2019). We predicted 38,039 and 29,160 proteins from G. yamadae 247 spermogonia and aecia unigenes, respectively.…”