Mitochondrial genomics of six cacao pathogens from the basidiomycete family Marasmiaceae

Authors: ALI, SHAHIN - University Of California, Davis; AMOAKO-ATTAH, ISHMAEL - Cocoa Research Institute Of Ghana; Shao, Jonathan; Meinhardt, Lyndel; Bailey, Bryan

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/1/2021
Publication Date: 10/28/2021
Citation: Ali, S., Amoako-Attah, I., Shao, J.Y., Meinhardt, L.W., Bailey, B.A. 2021. Mitochondrial genomics of six cacao pathogens from the basidiomycete family Marasmiaceae. Frontiers in Microbiology. 12:752094. https://doi.org/10.3389/fmicb.2021.752094.
DOI: https://doi.org/10.3389/fmicb.2021.752094

Interpretive Summary: Mushroom forming fungi can be major pathogens on important crops. Cacao, the source of chocolate, is unusual in that it is attacked by multiple species of one family of mushroom forming fungi, the Marasmiaceae. The diseases frosty pod rot (caused by Moniliophthora roreri) and witches’ broom (caused by Moniliophthora perniciosa) are associated with major disease losses on cacao in the Americas. Thread blight is an emerging disease in Ghana, Africa and is caused by at least four distinct species. New knowledge of the genetic similarities and differences among these species is needed if the diseases they cause are to be optimally managed. As part of a genome sequencing project we identified and characterized the mitochondrial genome sequences for all six species involved. Mitochondria serve as the energy producing compartments of higher life forms and carry genetic information required for that function. The six mitochondrial genomes all have unique structural aspects but relationships among the species were established based on their gene order. Specifically, the thread blight causing species Marasmius tenuissimus with Marasmius crinis-equi are closely related while the thread blight causing species Marasmius palmivorus is more closely related to the frosty pod and witches’ broom pathogens, leaving the fourth thread blight causing pathogen, Marasmiellus scandens, as a unique outlier. These results lead us to suggest adapting disease management methods for these pathogens accounting for the genetic relationships identified. The information provided will support scientists around the world in their efforts to understand and manage these diseases and many others caused by mushroom forming fungi.

Technical Abstract: Thread blight disease has recently been described as an emerging disease on cacao (Theobroma cacao) in Ghana. In Ghana, thread blight disease is caused by multiple species of the Marasmiaceae family: Marasmius tenuissimus, M. crinis-equi, M. palmivorus and Marasmiellus scandens. Interestingly, two additional members of the Marasmiaceae; Moniliophthora roreri (frosty pod rot) and Moniliophthora perniciosa (witches’ broom disease), are major pathogens of cacao in the Western hemisphere. It is important to accurately characterize the genetic relationships among these economically important species in support of their disease management. We used data from Illumina NGS-based genome sequencing efforts to study the mitochondrial genomes (mitogenomes) of the four cacao thread blight associated pathogens from Ghana and compared them with published mitogenomes of Mon. roreri and Mon. perniciosa. There is a remarkable interspecies variation in mitogenome size within the six cacao-associated Marasmiaceae species, ranging from 43,121 bp to 109,103 bp. The differences in genome lengths are primarily due to the number and lengths of introns, differences in intergenic space, and differences in the size and numbers of unidentified ORFs (uORF). Among 7 M. tenuissimus mitogenomes sequenced, there is variation in size and sequence pointing to divergent evolution patterns within the species. The intronic regions show a high degree of sequence variation compared to the conserved sequences of the 14 core genes. The intronic ORFs identified, regardless of species, encode GIY-YIG or LAGLIDADG domain-containing homing endonuclease genes. Phylogenetic relationships identified using the 14 core proteins largely mimic the phylogenetic relationships observed in gene order patterns grouping Marasmius tenuissimus with Marasmius crinis-equi, and Marasmius palmivorus with Mon. rorreri and Mon. perniciosa, leaving Marasmiellus scandens as an outlier. The results from this study provide evidence of independent expansion/contraction events and sequence diversification in each species and establish a foundation for further exploration of the evolutionary trajectory of the fungi in Marasmiaceae family.