Sexual reproduction is the null hypothesis for life cycles of rust fungi

McTaggart, Alistair R.; James, Timothy Y.; Idnurm, Alexander; Park, Robert; Shuey, Louise S.; Demers, Michelle N. K.; Aime, M. Catherine

doi:10.1371/journal.ppat.1010439

Cited by 8 publications

(8 citation statements)

References 25 publications

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“…McTaggart et al . (2022) proposed that an alternative hypothesis to explain why two dikaryotic rust isolates would share a common nucleus is through a duplicated fertilization event, where nectar from one pycnial infection of a single haploid genotype (haplotype A), was transferred to receptive hyphae of two different pycnial infections (haplotypes B and C), giving rise to dikaryotic sexual progeny of haplotypes AB and AC.…”

Section: Discussionmentioning

confidence: 99%

Extensive somatic nuclear exchanges shape global populations of the wheat leaf rust pathogenPuccinia triticina

Sperschneider

Hewitt

Lewis

et al. 2022

Preprint

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Non-sexual processes such as somatic nuclear exchange are postulated to play a role in the diversity of clonally reproducing dikaryotic rust fungi but have been difficult to detect due to the lack of genome resolution between the two haploid nuclei. We examined three nuclear-phased genome assemblies of Puccinia triticina, which causes wheat leaf rust disease. We found that the most recently emerged Australian lineage is derived by nuclear exchange between two pre-existing lineages, which originated in Europe and North America. Haplotype-specific phylogenetic analysis reveal that repeated somatic exchange events have shuffled haploid nuclei between long-term clonal lineages, leading to a global population representing different combinations of a limited number of haploid genomes. Thus, nuclear exchange seems to be the predominant mechanism generating diversity and the emergence of new strains in this otherwise clonal pathogen. Such genomics-accelerated surveillance of pathogen evolution paves the way for more accurate global disease monitoring.

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Section: Discussionmentioning

confidence: 99%

Extensive somatic nuclear exchanges shape global populations of the wheat leaf rust pathogenPuccinia triticina

Sperschneider

Hewitt

Lewis

et al. 2022

Preprint

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“…Culturable fungi are commonly used to study mating as compatibility can be tested in vitro . We know little about how mating is governed in obligate fungi, including rust fungi ( Pucciniales ) (Cuomo, et al 2017; Li, et al 2019; McTaggart, et al 2022) that cause rust diseases with economic impact for various crops, such as wheat, soybean, and coffee (Aime and McTaggart 2021). Rust fungi have multiple spore stages to complete their asexual and sexual life cycles.…”

Section: Introductionmentioning

confidence: 99%

“…Sexual recombination and somatic hybridisation may increase fitness of new isolates via pairing of novel haplotype combinations which can also lead to the avoidance of triggering resistance response of host plants. Understanding how rust fungi change is fundamental to disease management and to predict emerging genotypes (McTaggart, et al 2022).…”

Section: Introductionmentioning

confidence: 99%

Genome biology and evolution of mating type loci in four cereal rust fungi

Luo

McTaggart

Schwessinger

2023

Preprint

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Sex defining loci or chromosomes often contain large non-recombining regions. In Basidiomycota, two distinct gene loci confer mate compatibility. These loci encode for homeodomain (HD) transcription factors and pheromone receptor (PR)-ligand pairs. In some fungi these two loci are physically linked and give rise to large evolutionary strata with extensive recombination suppression. To date genome level mating type (MAT) loci analysis is lacking for obligate biotrophic basidiomycetes that depend on their host plants for survival, this includes the orderPucciniales. These economically important plant pathogens have long-term dikaryotic life-stages in which matched haploid nuclei must carry compatibleMATloci.Here we focus on fourPucciniacereal rust species, includingPuccinia graminisf.sptritici,P. striiformisf.sptritici,P. triticinaandP. coronataf.spavenae, which infect major cereals including wheat and oat. We identifiedMATlocations on two separate chromosomes that supports previous hypotheses of a tetrapolar mating system in thePucciniales.HDloci displayed largely conserved macrosynteny among species and were not suppressed for recombination. Consistently,HDtranscription factor genes showed no trans-specific polymorphisms between species. Regions, surrounding thePRloci however, displayed extensive genomic degeneration, signs of recombination suppression and were found to be linked to centromeres in some species. Expression analysis suggests that bothMATloci are involved in nuclear pairing during spore formation in the asexual cycle. Together, our study provides insights into the evolution ofMATloci since speciation of key pathogenicPucciniaspecies. This detailed understanding is important to predict the possible combinations of nuclear pairs that can arise via sexual reproduction, somatic recombination, or di-om mating to enable the evolution of newly virulent isolates of these agriculturally important plant pathogens.

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“…The process underlying these chromosome dynamics remains unclear. Fusarium oxysporum has long been considered to evolve strictly asexually (Gordon & Martyn, 1997); however, the presence of an active sexual cycle in F. oxysporum populations has recently been proposed (McTaggart et al ., 2022; Fayyaz et al ., 2023) and we similarly observe reticulation between strains that caused FWB (Fig. S10), which supports an evolutionary history in which ancient or infrequent sexual recombination is followed by clonal expansion of selected lineages.…”

Section: Discussionmentioning

confidence: 99%

Segmental duplications drive the evolution of accessory regions in a major crop pathogen

van Westerhoven,

Aguilera‐Galvez,

Nakasato‐Tagami

et al. 2024

New Phytologist

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Summary Many pathogens evolved compartmentalized genomes with conserved core and variable accessory regions (ARs) that carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such ARs, often spanning entire chromosomes. The presence of specific ARs influences the host range, and horizontal transfer of ARs can modify the pathogenicity of the receiving strain. However, how these ARs evolve in strains that infect the same host remains largely unknown. We defined the pan‐genome of 69 diverse F. oxysporum strains that cause Fusarium wilt of banana, a significant constraint to global banana production, and analyzed the diversity and evolution of the ARs. Accessory regions in F. oxysporum strains infecting the same banana cultivar are highly diverse, and we could not identify any shared genomic regions and in planta‐induced effectors. We demonstrate that segmental duplications drive the evolution of ARs. Furthermore, we show that recent segmental duplications specifically in accessory chromosomes cause the expansion of ARs in F. oxysporum. Taken together, we conclude that extensive recent duplications drive the evolution of ARs in F. oxysporum, which contribute to the evolution of virulence.

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Sexual reproduction is the null hypothesis for life cycles of rust fungi

Cited by 8 publications

References 25 publications

Extensive somatic nuclear exchanges shape global populations of the wheat leaf rust pathogenPuccinia triticina

Extensive somatic nuclear exchanges shape global populations of the wheat leaf rust pathogenPuccinia triticina

Genome biology and evolution of mating type loci in four cereal rust fungi

Segmental duplications drive the evolution of accessory regions in a major crop pathogen

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