Loss of PWT7, Located on a Supernumerary Chromosome, Is Associated with Parasitic Specialization of Pyricularia oryzae on Wheat

Abstract

Pyricularia oryzae, a blast fungus of gramineous plants, is composed of various host-genus specific pathotypes. The avirulence of an Avena isolate on wheat is conditioned by PWT3 and PWT4. We isolated the third avirulence gene from the Avena isolate and designated it as PWT7. PWT7 was effective as an avirulence gene only at the seedling stage or on leaves. PWT7 homologs were widely distributed in a subpopulation of the Eleusine pathotype and the Lolium pathotype but completely absent in the Triticum pathotype (the wheat blast fungus). The PWT7 homolog found in the Eleusine pathotype was one of the five genes involved in its avirulence on wheat. A comparative analysis of distribution of PWT7 and the other two genes previously identified in the Eleusine pathotype suggested that, in the course of parasitic specialization toward the wheat blast fungus, a common ancestor of the Eleusine, Lolium, Avena, and Triticum pathotypes first lost PWT6, secondly PWT7, and finally the function of PWT3. PWT7 or its homologs were located on core chromosomes in Setaria and Eleusine isolates but on supernumerary chromosomes in Lolium and Avena isolates. This is an example of inter-chromosomal translocations of effector genes between core and supernumerary chromosomes.

Pyricularia oryzae: Lab star and field scourge

“…Genetic analysis of crosses between isolates from different host‐specific lineages have demonstrated that the incompatibility of P. oryzae on nonhost species is in most cases controlled by relatively few genes, generally one to three (Cruz & Valent, 2017 ; Murakami et al., 2003 ; Takabayashi et al., 2002 ; Tosa et al., 2006 ; Valent & Chumley, 1991 ). Several of these genes code for effector proteins such as PWL1 and PWL2 that control pathogenicity towards Eragrostis curvula (weeping lovegrass) or PWT3, PWT4 or PWT7 that control pathogenicity on wheat (Asuke et al., 2023 ; Inoue et al., 2017 ; Sweigard et al., 1995 ). In all studied cases, it was the loss‐of‐function alleles that conferred compatibility on the new host, suggesting that the host specificity of the blast fungus is frequently determined by immune receptor‐mediated detection of virulence effectors in nonhost plants.…”

Recent co-evolution of two pandemic plant diseases in a multi-hybrid swarm

“…The evolutionary history of WB yields new insights in this regard by building on foundational work from Tosa and colleagues who identified five PWT genes that determine P. oryzae avirulence on wheat 33,37,50 . After surveying allele distributions for two cloned genes, they proposed an evolutionary model where functional losses of PWT6 and currently unknown PWT genes allowed an Eleusine pathogen to colonize rwt3 wheat, probably via an intermediate Lolium host 32 .…”

Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages

“…While these instances highlight HGT as a possible driver of genetic variation in the blast fungus, the exact mechanisms facilitating HGT remain unclear. In addition to gene transfer, mChr have been associated with virulence gene reshuffling and recombination with core chromosomes (Kusaba et al 2014;Peng et al 2019;Langner et al 2021;Asuke et al 2023;Gyawali et al 2023), indicating that horizontal mChr transfer could be instrumental in driving genomic innovation. In this study, we provide evidence for multiple horizontal mini-chromosome transfer events involving clonal lineages of the rice blast fungus M. oryzae that occurred under field conditions.…”

“…The adaptive role of mChr in plant pathogenic fungi is underpinned by their correlation to virulence in various pathogen-host systems (Miao et al 1991; Kistler 1996; Han et al 2001; Akagi et al 2009; Ma et al 2010; Chuma et al 2011; Balesdent et al 2013; van Dam et al 2017; Habig et al 2017; Bhadauria et al 2019; Henry et al 2021; Asuke et al 2023). In addition, variation in virulence has been partly attributed to the horizontal transfer of mChr (Mehrabi et al 2011).…”