Analylis of the genetic diversity of the soybean rust pathogen Phakopsora pachyrhizi revelas two major evolutionary lineages

Authors: ROCHA, V.D. - Brazilian Agricultural Research Corporation (EMBRAPA); FERREIRA, E. G. C. - Brazilian Agricultural Research Corporation (EMBRAPA); CASTANHO, F. M. - Brazilian Agricultural Research Corporation (EMBRAPA); KUWAHARA, M.K. - Brazilian Agricultural Research Corporation (EMBRAPA); GODOY, C. - Brazilian Agricultural Research Corporation (EMBRAPA); MEYER, M. - Brazilian Agricultural Research Corporation (EMBRAPA); Pedley, Kerry; VOEGELE, R.T. - University Of Hohenheim; GRIGORIEV, I.V. - Department Of Energy Joint Genome; LIPZEN, A. - Department Of Energy Joint Genome; BARRY, K. - Department Of Energy Joint Genome; LOEHRER, M - Aachen University; SCHAFFRATH, U. - Aachen University; SIRVEN, C. - Bayer Biosciences; DUPLESSIS, S. - Université De Lorraine; GUIMARÃES, F.C.G - Brazilian Agricultural Research Corporation (EMBRAPA)

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2025
Publication Date: 5/2/2025
Citation: Rocha, V., Ferreira, E., Castanho, F., Kuwahara, M., Godoy, C., Meyer, M., Pedley, K.F., Voegele, R., Grigoriev, I., Lipzen, A., Barry, K., Loehrer, M., Schaffrath, U., Sirven, C., Duplessis, S., Guimarães, F. 2025. Analylis of the genetic diversity of the soybean rust pathogen Phakopsora pachyrhizi revelas two major evolutionary lineages. Fungal Genetics and Biology. 179:103990. https://doi.org/10.1016/j.fgb.2025.103990.
DOI: https://doi.org/10.1016/j.fgb.2025.103990

Interpretive Summary: Soybean rust, caused by the fungal pathogen Phakopsora pachyrhizi, is an aggressive disease of soybeans and other legumes. The disease negatively impacts soybean production, causing yield losses up to 80% under environmental conditions that are favorable to disease development. The control and management of the disease is particularly challenging due to the high variability in virulence levels of the pathogen, and the potential occurrence of multiple pathogenic races. Recently developed genome resources and a diverse panel of Phakopsora pachyrhizi isolates were used to gain insight into the evolution and population structure of the soybean rust pathogen. This information will be used to guide soybean breeding programs aimed at matching resistant soybean lines with local populations of the pathogen.

Technical Abstract: Phakopsora pachyrhizi, an obligate biotrophic rust fungus, is the causal agent of Asian Soybean Rust (ASR) disease. Here, we utilized whole-genome data to explore the evolutionary patterns and population structure across 45 P. pachyrhizi isolates collected from 1972 to 2017 within diverse geographic regions worldwide. We also characterized in-silico mating-type (MAT) genes of P. pachyrhizi, utilizing the predicted proteome of three isolates, to investigate the sexual compatibility system. Our molecular phylogenetic analysis in P. pachyrhizi inferred two distinct evolutionary lineages structured within a temporal scale, with lineage Pp1 grouping isolates obtained from 1972 to 1994, while more recently collected isolates formed a second lineage, Pp2. We found high levels of genetic diversity in lineage Pp1, whereas lineage Pp2 exhibited a strong clonal genetic structure, with significantly lower diversity. The widespread propagation of P. pachyrhizi clonal spores across soybean-growing regions likely explains the absence of a large-scale spatial genetic structure within each lineage. Two independent isolates (TW72-1 and AU79-1) showed moderate levels of genetic admixture, suggesting potential somatic hybridization between the two P. pachyrhizi lineages. We observed no clear congruence between virulence levels of P. pachyrhizi isolates and their phylogenetic patterns. Our findings support a probable tetrapolar mating system in P. pachyrhizi. The localization of conserved MAT loci was predicted in both primary and secondary haplotypes of P. pachyrhizi genomes. Based on publicly available transcriptome data, we discovered that multiple MAT genes of P. pachyrhizi were highly expressed during the late stages of soybean infection.