Correlation of Genomic Compartments with Contrastive Modes of Functional Losses of Host Specificity Determinants During Pathotype Differentiation in <i>Pyricularia oryzae</i>

Asuke, Soichiro; Magculia, Nicole John; Inoue, Yushi; Vy, Trinh Thi Phuong; Tosa, Yukio

doi:10.1094/mpmi-12-20-0339-r

Cited by 4 publications

(7 citation statements)

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“…Using chromosome-level, reference-guided genome assemblies, we first determined that the correct chromosomal position for PWT6, and the corresponding null locus, is in the middle of chromosome 5 (fig. S8A), and not the end of chromosome 3 as originally reported (47). A quick inspection of PoL1's haplotype at this locus told us that the donor was probably the PoU1 parent and, consistent with this prediction, all PoU1 isolates were found to lack PWT6.…”

Section: Sequential Admixture Drove Broad Infection Capability On Wheat Through Multiple Independent Contributions Of Null/non-functionalsupporting

confidence: 57%

“…Prior work has shown that successful infection of wheat requires the loss or inactivation of the PWT6 and PWT3 host-specificity genes that would normally trigger resistance in wheat containing the corresponding resistance genes ( 29, 47 ). Therefore, we sought to understand the dynamics of these genes in the context of PoT/PoL evolution.…”

Section: Resultsmentioning

confidence: 99%

“…i) PWT6 was deleted in the PoU1 lineage and was donated to PoT/PoL in admixture 1 . PWT6 is present in P. oryzae isolates from Eleusine and Eragrostis , yet absent from PoL, which prompted the conclusion that the gene was lost when PoL branched from the Eleusine lineage ( 47 ). However, because our data show that PoL evolved through lineage convergence and not branching, we suspected that the PWT6 was already missing in the PoU1 lineage and donated to PoL in admixture 1.…”

Section: Resultsmentioning

confidence: 99%

“…Rather fittingly, thinking on wheat blast evolution has paralleled that in evolutionary biology. In line with early theory, prior data were interpreted according to a model where host-specialized lineages differentiated in a bifurcating fashion through the gradual and step-wise accumulation of mutations in host-specificity factors ( 47 ). The differentiation of Lolium pathotypes from the PoE lineage was associated with the loss of PWT6 , and the subsequent evolution of wheat blast was proposed to have involved an initial host jump by a wheat-adapted Lolium pathogen, followed by further adaptations involving mutations in PWT3 ( 29 ).…”

Section: Discussionmentioning

confidence: 99%

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Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

Rahnama

Condon

Ascari

et al. 2021

Preprint

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Adaptive radiations fuel speciation and are characterized by rapid genetic diversification and expansion into new ecological niches. Historically, these processes were believed to be driven by selection on novel mutations but genomic analyses now indicate that standing variation and gene flow often have prominent roles. How “old” variation is combined, however, and its resulting genetic architecture within newly-adapted populations is not well understood. We reconstructed a recent radiation in the fungus, Pyricularia oryzae, that spawned a population pathogenic to eleven grass genera, and caused two new plant diseases: wheat blast - already a serious threat to global agriculture - and gray leaf spot of ryegrasses. We show that the new population evolved in a multi-hybrid swarm using only the standing variation that was present in seven individuals from five distinct, host-specialized lineages. Sexual and parasexual recombination within the swarm reassorted key host-specificity factors and generated more diversity in possibly just a few weeks than existing lineages had accumulated over hundreds to thousands of years. We suggest that the process was initiated by sexual opportunity arising when a fertile fungal strain was imported into Brazil on Urochloa introduced as forage for beef production; and we further contend that the host range expansion was largely fortuitous, with host selection playing little, if any, role in driving the process. Finally, we believe that our findings point to an overlooked role for happenstance in creating situations that allow organisms to skirt rules that would normally hold evolution in check.Commercial Endorsement DisclaimerMention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.Equal Opportunity/Non-Discrimination StatementUSDA is an equal opportunity provider and employer.

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Section: Sequential Admixture Drove Broad Infection Capability On Wheat Through Multiple Independent Contributions Of Null/non-functionalsupporting

confidence: 57%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

Rahnama

Condon

Ascari

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…The prevailing model for WB evolution holds that it involved sequential loss/mutation of key host specificity genes, which allowed an Eleusine pathogen to jump hosts-first onto Lolium, then onto wheat lacking the RWT3 resistance gene and, finally, onto RWT3 wheat 32,33 . However, this could not explain how such high levels of genetic diversity arose in a population that had no obvious existence before 1985.…”

mentioning

confidence: 99%

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

Rahnama,

Condon,

Ascari

et al. 2023

Nat Ecol Evol

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Most plant pathogens exhibit host specificity but when former barriers to infection break down, new diseases can rapidly emerge. For a number of fungal diseases, there is increasing evidence that hybridization plays a major role in driving host jumps. However, the relative contributions of existing variation versus new mutations in adapting to new host(s) is unclear. Here we reconstruct the evolutionary history of two recently emerged populations of the fungus Pyricularia oryzae that are responsible for two new plant diseases: wheat blast and grey leaf spot of ryegrasses. We provide evidence that wheat blast/grey leaf spot evolved through two distinct mating episodes: the first occurred ~60 years ago, when a fungal individual adapted to Eleusine mated with another individual from Urochloa. Then, about 10 years later, a single progeny from this cross underwent a series of matings with a small number of individuals from three additional host-specialized populations. These matings introduced non-functional alleles of two key host-specificity factors, whose recombination in a multi-hybrid swarm probably facilitated the host jump. We show that very few mutations have arisen since the founding event and a majority are private to individual isolates. Thus, adaptation to the wheat or Lolium hosts appears to have been instantaneous, and driven entirely by selection on repartitioned standing variation, with no obvious role for newly formed mutations.

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

Asuke

Horie

Komatsu

et al. 2023

MPMI

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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.

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Correlation of Genomic Compartments with Contrastive Modes of Functional Losses of Host Specificity Determinants During Pathotype Differentiation in Pyricularia oryzae

Cited by 4 publications

References 51 publications

Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

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

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

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