The cacao pathogen Moniliophthora roreri (Marasmiaceae) possesses biallelic A and B mating loci but reproduces clonally

Abstract

The cacao pathogen Moniliophthora roreri belongs to the mushroom-forming family Marasmiaceae, but it has never been observed to produce a fruiting body, which calls to question its capacity for sexual reproduction. In this study, we identified potential A (HD1 and HD2) and B (pheromone precursors and pheromone receptors) mating genes in M. roreri. A PCR-based method was subsequently devised to determine the mating type for a set of 47 isolates from across the geographic range of the fungus. We developed and generated an 11-marker microsatellite set and conducted association and linkage disequilibrium (standardized index of association, I A s ) analyses. We also performed an ancestral reconstruction analysis to show that the ancestor of M. roreri is predicted to be heterothallic and tetrapolar, which together with sliding window analyses support that the A and B mating loci are likely unlinked and follow a tetrapolar organization within the genome. The A locus is composed of a pair of HD1 and HD2 genes, whereas the B locus consists of a paired pheromone precursor, Mr_Ph4, and receptor, STE3_Mr4. Two A and B alleles but only two mating types were identified. Association analyses divided isolates into two well-defined genetically distinct groups that correlate with their mating type; I A s values show high linkage disequilibrium as is expected in clonal reproduction. Interestingly, both mating types were found in South American isolates but only one mating type was found in Central American isolates, supporting a prior hypothesis of clonal dissemination throughout Central America after a single or very few introductions of the fungus from South America.

Fungal Sex: The Basidiomycota

“…Interestingly, whereas synteny analysis of the surrounding regions indicates that the separation of the two HD subloci in S. commune emerged via transposition of the two gene clusters, the extant arrangement in F. velutipes was driven by two large inversions (95). Other exceptions to the typical MIP – HD1/HD2 – β-fg gene arrangement were observed in the cacao pathogen Moniliophthora roreri , where both MIP and β-fg are located 40 and 60 kb upstream of HD1 / HD2 (105), respectively, and in the Shiitake mushroom, Lentinula edodes , where MIP is distant to the HD locus (106). Gene order conservation at the P/R locus is also observed among Agaricomycetes, although to a lesser extent compared to the HD locus.…”

Moniliophthora roreri, causal agent of cacao frosty pod rot

“…(). More recently, Díaz‐Valderrama and Aime (), using a different isolate from T. gileri , found no morphological or molecular differences.…”

“…Mp (biotype C) evolved to be self‐compatible (homothallic) despite the presence of A and B mating type genes (Kües and Navarro‐González, ). Díaz‐Valderrama and Aime () identified A and B mating type genes in Mr . Only one mating type was found in Central America, demonstrating their lack of critical importance in Mr spread (Díaz‐Valderrama and Aime, ).…”

“…Díaz‐Valderrama and Aime () identified A and B mating type genes in Mr . Only one mating type was found in Central America, demonstrating their lack of critical importance in Mr spread (Díaz‐Valderrama and Aime, ). Clearly, if meiosis is to be considered as important in Mr biology, additional evidence is required.…”

“…We have pathogen (Meinhardt et al ., ) and host (Argout et al ., ) draft genomes and transcriptomes (Meinhardt et al ., ). Our understanding of the pathogen's genetic diversity makes it clear that genetic recombination in Mr is rare to non‐existent (Ali et al ., ; Díaz‐Valderrama and Aime, ; Phillips‐Mora et al ., ). The assessment of Mr genetic diversity and the molecular interactions with cacao currently drive our interpretation of the biology and will be critical to the management of FPR in the future.…”