The genetic diversity of the soybean rust pathogenPhakopsora pachyrhizihas been driven by two major evolutionary lineages
Authors: Rocha Vinicius Delgado da , Ferreira Everton Geraldo Capote , Castanho Fernanda Machado , Kuwahara Marcia Kamogae , Godoy Cláudia Vieira , Meyer Maurício Conrado , Pedley Kerry F. , Voegele Ralf T. , Lipzen Anna , Barry Kerrie , Grigoriev Igor V. , Loehrer Marco , Schaffrath Ulrich , Sirven Catherine , Duplessis Sebastien , Marcelino-Guimarães Francismar Corrêa 
Published: October 2024

ABSTRACTPhakopsora 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 45P. pachyrhiziisolates collected from 1972 to 2017 from diverse geographic regions worldwide. We also characterizedin-silicomating-type (MAT) genes ofP. pachyrhizi, in the predicted proteome of three isolates, to investigate the sexual compatibility system. Our molecular phylogenetic analysis inP. pachyrhiziinferred two distinct evolutionary lineages structured on 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 a significant lower diversity. The widespread propagation ofP. pachyrhiziclonal 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 twoP. pachyrhizilineages. We observed no clear congruence between virulence levels ofP. pachyrhiziisolates and their phylogenetic patterns. Our findings support a probable tetrapolar mating system inP. pachyrhizi. Taken together, our study offers new insights into the evolutionary history ofP. pachyrhiziand demonstrates that multipleMATgenes are highly expressed during the later stages of soybean infection, suggesting their potential role in the formation of urediniospores within the life cycle ofP. pachyrhizi.AUTHOR SUMMARYThe Asian Soybean Rust (ASR) disease, caused by basidiomycetes fungusP. pachyrhizi, represents a critical threat to soybean crops worldwide. With the recent availability of high-quality genome assemblies forP. pachyrhizi, we are committed to exploring the genetic diversity of this destructive pathogen. This study analyzed whole-genome resequencing data fromP. pachyrhiziisolates collected over several decades in various geographic regions. We identified recent diversification patterns inP. pachyrhizi, with two major lineages. The origin of the two lineages is likely due to temporal shifts in the genetic structure ofP. pachyrhizi. Additionally, we investigated the genes responsible for sexual compatibility, known as mating-type (MAT) genes. Transcriptome data indicated thatMATgenes are actively expressed during the later stages of theP. pachyrhizi-soybean infection. We conclude that the evolutionary dynamic ofP. pachyrhiziis shaped by divergent lineages, which exhibit varying levels of virulence on differential soybean lines containing ASR resistance genes.