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
Brazilian Agricultural Research Corporation - National Soybean Research Center (Embrapa Soja), Paraná, Brazil.
Brazilian Agricultural Research Corporation - National Soybean Research Center (Embrapa Soja), Paraná, Brazil; 2Blades, Evanston, IL, USA; The Sainsbury Laboratory, University of East Anglia, Norwich, UK.
Fungal Genet Biol. 2025 Jun;179:103990. doi: 10.1016/j.fgb.2025.103990. Epub 2025 May 2.
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 from diverse geographic regions worldwide. We also characterized in-silico mating-type (MAT) genes of P. pachyrhizi, in 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 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 higher levels of genetic diversity in lineage Pp1, whereas lineage Pp2 exhibited a strong clonal genetic structure, with a significant 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. Taken together, our study offers new insights into the evolutionary history of P. pachyrhizi and demonstrates that multiple MAT genes are highly expressed during the later stages of soybean infection, suggesting their potential role in the formation of urediniospores within the life cycle of P. pachyrhizi.
豆薯层锈菌是一种专性活体寄生锈菌，是亚洲大豆锈病（ASR）的病原菌。在此，我们利用全基因组数据，探索了1972年至2017年间从全球不同地理区域收集的45株豆薯层锈菌分离株的进化模式和种群结构。我们还对三个分离株预测蛋白质组中的豆薯层锈菌的计算机模拟交配型（MAT）基因进行了表征，以研究其有性亲和系统。我们对豆薯层锈菌的分子系统发育分析推断出两个在时间尺度上构建的不同进化谱系，谱系Pp1包含1972年至1994年获得的分离株，而最近收集的分离株形成了第二个谱系Pp2。我们发现谱系Pp1中的遗传多样性水平较高，而谱系Pp2表现出强烈的克隆遗传结构，多样性显著较低。豆薯层锈菌克隆孢子在大豆种植区的广泛传播可能解释了每个谱系内缺乏大规模空间遗传结构的原因。两个独立的分离株（TW72-1和AU79-1）表现出中等水平的遗传混合，表明两个豆薯层锈菌谱系之间可能存在体细胞杂交。我们观察到豆薯层锈菌分离株的毒力水平与其系统发育模式之间没有明显的一致性。我们的研究结果支持豆薯层锈菌可能存在四极性交配系统。综上所述，我们的研究为豆薯层锈菌的进化历史提供了新的见解，并表明多个MAT基因在大豆感染后期高度表达，暗示了它们在豆薯层锈菌生命周期中夏孢子形成中的潜在作用。
