Leaf Rust in Rye: From Pathogen Biology to Host Defence and Resistance Breeding

Leaf rust (LR) caused by Puccinia recondita f. sp. secalis (Prs) is considered one of the most dangerous rye (Secale cereale L.) diseases, causing yield losses exceeding 35%. This review summarizes all currently available data about this disease: pathogen characteristics (including its life cycle, natural variation and disease symptoms), resistance resources and the background of the plant immune response at the genome, transcriptome and metabolome levels. The research conducted so far has allowed the identification of dozens of genes that play a significant role in the rye immune response to Prs infection. Among them, genes encoding NBS-LRR proteins (including SECCE1Rv1G0014220, the most likely Pr3 candidate), glycosyltransferase, β-1,3-glucanase, 1-deoxy-D-xylulose 5-phosphate synthase, β-1,3-glucanase, UDP-glycosyltransferase, pathogenesis-related protein 1, ammonium transporter and cytochrome P450 enzymes are candidates for seedling and all-stage resistance, whereas ScLr_ABC25 currently represents the most promising candidate associated with adult-plant resistance. Among the metabolites differentially accumulated in response to Prs, those related to phenylpropanoids, diterpenoids and thiamine branches seem to play the most important role in the immune response. Finally, we suggest how the so far acquired knowledge about rye-Prs interaction can be used in the modern breeding programs aimed at obtaining cultivars with enhanced resistance to LR, e.g. through the use of functional gene markers and/or metabolic biomarker assisted selection and, in the more distant future, by developing and applying new genomic techniques for precise editing of resistance and susceptibility genes, engineering synthetic immune receptors and decoys, and pan-genomic exploration for identification of rare or lineage-specific resistance alleles.