The Bcvic1 and Bcvic2 vegetative incompatibility genes in Botrytis cinerea encode proteins with domain architectures involved in allorecognition in other filamentous fungi

Arshed, Saadiah; Cox, Murray P.; Beever, Ross E.; Parkes, Stephanie L.; Pearson, Michael N.; Bowen, Joanna K.; Templeton, Matthew D.

doi:10.1016/j.fgb.2023.103827

Cited by 4 publications

(7 citation statements)

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“…In yeast, this gene functions in vesicle fusion during exocytosis ( Kustermann et al 2017 : 1; Masgrau et al 2017 : 1). Interestingly, a similar pairing has recently been described in the het genes of the plant pathogen Botrytis cinerea : Bcvic1 , a NACHT + Ankyrin encoding gene, and Bcvic2, which encodes a SNARE syntaxin protein ( Arshed et al 2023 ). These SNARE domains are involved in anchoring cargoes to membranes and are also known from the sec -9/SNARE system in N. crassa , and het-Z of Podospora anserina, which both involve an NLR type protein and a SNARE protein ( Heller et al 2018 ).…”

Section: Discussionmentioning

confidence: 52%

The Narrow Footprint of Ancient Balancing Selection Revealed by Heterokaryon Incompatibility Genes in Aspergillus fumigatus

Auxier,

Zhang,

Marquez

et al. 2024

Molecular Biology and Evolution

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In fungi, fusion between individuals leads to localized cell death, a phenomenon termed heterokaryon incompatibility. Generally, the genes responsible for this incompatibility are observed to be under balancing selection resulting from negative frequency-dependent selection. Here, we assess this phenomenon in Aspergillus fumigatus, a human pathogenic fungus with a very low level of linkage disequilibrium as well as an extremely high crossover rate. Using complementation of auxotrophic mutations as an assay for hyphal compatibility, we screened sexual progeny for compatibility to identify genes involved in this process, called het genes. In total, 5/148 (3.4%) offspring were compatible with a parent and 166/2142 (7.7%) sibling pairs were compatible, consistent with several segregating incompatibility loci. Genetic mapping identified five loci, four of which could be fine mapped to individual genes, of which we tested three through heterologous expression, confirming their causal relationship. Consistent with long-term balancing selection, trans-species polymorphisms were apparent across several sister species, as well as equal allele frequencies within A. fumigatus. Surprisingly, a sliding window genome-wide population-level analysis of an independent dataset did not show increased Tajima’s D near these loci, in contrast to what is often found surrounding loci under balancing selection. Using available de novo assemblies, we show that these balanced polymorphisms are restricted to several hundred base pairs flanking the coding sequence. In addition to identifying the first het genes in an Aspergillus species, this work highlights the interaction of long-term balancing selection with rapid linkage disequilibrium decay.

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Section: Discussionmentioning

confidence: 52%

The Narrow Footprint of Ancient Balancing Selection Revealed by Heterokaryon Incompatibility Genes in Aspergillus fumigatus

Auxier,

Zhang,

Marquez

et al. 2024

Molecular Biology and Evolution

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“…The Neurospora het-c/pin-c allorecognition locus conforms to such a scenario as it has evolved as a consequence of a rearrangement event whereby the pin-c HET-domain gene was inserted near the het-c locus (92). This hypothesis can also explain the convergent linkage of distinct NLR-encoding genes to sec9 SNARE homologs at allorecognition loci in Botrytis , Cryphonectria , Neurospora , and Podospora (14, 39, 41). Alternatively, the partner genes evolving into het -alleles might have already been linked at the time of emergence of the incompatibility system (as a result of a pre-existing functional coupling).…”

Section: Discussionmentioning

confidence: 95%

“…These studies led successively to the molecular characterization of het-S (27), het-C (28), het-E (29), het-D (30), het-R (31), het-Z (14), het-Q (32) and het-V (13). Het genes have also been isolated in Neurospora crassa (14, 17, 33–38) and Cryphonectria parasitica (39, 40), and more recently in Aspergillus fumigatus (16) and Botrytis cinerea (41). Collectively, these studies revealed that a diversity of protein architectures control incompatibility-driven cell death.…”

Section: Introductionmentioning

confidence: 99%

het-Ballorecognition inPodospora anserinais determined by pseudo-allelic interaction of genes encoding a HET and lectin fold domain protein and a PII-like protein

Clavé,

Dheur,

Ament-Velásquez

et al. 2023

Preprint

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Filamentous fungi display allorecognition genes that trigger regulated cell death (RCD) when strains of unlike genotype fuse.Podospora anserinais one of several model species for the study of this allorecognition process termed heterokaryon or vegetative incompatibility. Incompatibility restricts transmission of mycoviruses between isolates. InP. anserina, genetic analyses have identified nine incompatibility loci, termedhetloci. Here we set out to clone the genes controllinghet-Bincompatibility.het-Bdisplays two incompatible alleles,het-B1andhet-B2. We find that thehet-Blocus encompasses two adjacent genes,BhandBpthat exist as highly divergent allelic variants (Bh1/Bh2andBp1/Bp2) in the incompatible haplotypes.Bhencodes a protein with an N-terminal HET domain, a cell death inducing domain bearing homology to Toll/interleukin-1 receptor (TIR) domains and a C-terminal domain with a predicted lectin fold. TheBpproduct is homologous to PII-like proteins, a family of small trimeric proteins acting as sensors of adenine nucleotides in bacteria. We show that although thehet-Bsystem appears genetically allelic, incompatibility is in fact determined by the non-allelicBh1/Bp2interaction while the reciprocalBh2/Bp1interaction plays no role in incompatibility. The highly divergent C-terminal lectin fold domain of BH determines recognition specificity. Population studies and genome analyses indicate thathet-Bis under balancing selection with trans-species polymorphism, highlighting the evolutionary significance of the two incompatible haplotypes. In addition to emphasizing anew the central role of TIR-like HET domains in fungal RCD, this study identifies novel players in fungal allorecognition and completes the characterization of the entirehetgene set in that species.Author summaryMany cellular life forms display genetic systems that protect individuality and discriminate conspecific self from non-self. In filamentous fungi, cell fusion events between strains are under check by specific allorecognition genes that trigger regulated cell death upon detection of non-self. The role of incompatibility is to restrict mycovirus transmission and conspecific parasitism.Podospora anserina, a good model for the study of this form of allorecognition, harbors nine incompatibilityhetloci. Previous studies have revealed that these genes can be homologous to genes with immune functions in other phyla including bacteria, plants and animals. We have clonedhet-B,the last of the ninehetgenes that remained to be identified and found that it is a complex locus comprising two adjacent genesBhandBp. BH displays an N-terminal HET domain (related to TIR domains) and a C-terminal domain with a predicted lectin fold. BP is homologous to PII-like proteins, known bacterial metabolite sensors. Intriguingly, despite apparent genetic allelism, incompatibility is dictated by the non-allelicBh/Bpinteraction. This study stresses the reoccurring involvement of HET domains in fungal RCD and signs completion of the characterization of the entire set ofhetloci in that species, enabling a comparative analysis of the different genetic architectures underlying allorecognition.

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“…In filamentous fungi, this process is typically termed vegetative (or heterokaryon) incompatibility (VIC) 1 , 2 , wherein contact between genetically incompatible fungal strains triggers a non-self recognition reaction preventing any subsequent hyphal fusion via numerous pathways including programmed cell death (PCD) 1 , 2 . Studies exploring the molecular mechanisms underpinning self/non-self recognition in filamentous fungi have primarily focused on ascomycetes such as Neurospora crassa , Podospora anserina , Cryphonectria parasitica , and Botrytis cinerea 3 – 12 . The genetic loci determining self/non-self recognition are traditionally termed het ( het erokaryon) or vic ( v egetative i n c ompatibility).…”

Section: Introductionmentioning

confidence: 99%

“…Conversely, strains harboring different alleles are incompatible and belong to different VCGs 1 , 9 , 13 . Genes involved in the self/non-self recognition reaction encode heterotrimeric guanine nucleotide-binding proteins (G proteins), proteins involved in generation and scavenging of reactive oxygen species (ROS), and proteins containing HET domains, nucleotide oligomerization domain-like receptors, and cell wall remodeling checkpoint regulators 5 , 11 , 12 , 14 , 15 . Fundamentally, the self/non-self reaction functions akin to a rudimentary innate immune system, restricting the transmission of deleterious factors, including mycoviruses, between fungal strains, and thereby enhancing organismal fitness in natural environments 11 .…”

Section: Introductionmentioning

confidence: 99%

Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission

Hai,

Li,

Jiang

et al. 2024

Nat Commun

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Non-self recognition is a fundamental aspect of life, serving as a crucial mechanism for mitigating proliferation of molecular parasites within fungal populations. However, studies investigating the potential interference of plants with fungal non-self recognition mechanisms are limited. Here, we demonstrate a pronounced increase in the efficiency of horizontal mycovirus transmission between vegetatively incompatible Sclerotinia sclerotiorum strains in planta as compared to in vitro. This increased efficiency is associated with elevated proline concentration in plants following S. sclerotiorum infection. This surge in proline levels attenuates the non-self recognition reaction among fungi by inhibition of cell death, thereby facilitating mycovirus transmission. Furthermore, our field experiments reveal that the combined deployment of hypovirulent S. sclerotiorum strains harboring hypovirulence-associated mycoviruses (HAVs) together with exogenous proline confers substantial protection to oilseed rape plants against virulent S. sclerotiorum. This unprecedented discovery illuminates a novel pathway by which plants can counteract S. sclerotiorum infection, leveraging the weakening of fungal non-self recognition and promotion of HAVs spread. These promising insights provide an avenue to explore for developing innovative biological control strategies aimed at mitigating fungal diseases in plants by enhancing the efficacy of horizontal HAV transmission.

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The Bcvic1 and Bcvic2 vegetative incompatibility genes in Botrytis cinerea encode proteins with domain architectures involved in allorecognition in other filamentous fungi

Cited by 4 publications

References 93 publications

The Narrow Footprint of Ancient Balancing Selection Revealed by Heterokaryon Incompatibility Genes in Aspergillus fumigatus

The Narrow Footprint of Ancient Balancing Selection Revealed by Heterokaryon Incompatibility Genes in Aspergillus fumigatus

het-Ballorecognition inPodospora anserinais determined by pseudo-allelic interaction of genes encoding a HET and lectin fold domain protein and a PII-like protein

Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission

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