Clonal Propagation of Moniliophthora roreri and the emergence of unique lineages with distinct genomes during range expansion

Authors: MINIO, ANDREA - University Of California, Davis; ALI, SHAHIN - University Of California, Davis; Cohen, Stephen; FIGUEROA-BALDERAS, ROSA - University Of California, Davis; CARRIEL, DENNY - M & M Mars Company - Brazil; DAHYANA, BRITTO - M & M Mars Company - Brazil; CONRAD STACK, JOSEPH - Mars, Inc; BARUAH, INDRANI - Non ARS Employee; JEAN-PHILIPPE, MARELLI - Mars Chocolate North America; CANTU, DARIO - University Of California, Davis; Bailey, Bryan

Submitted to: Genes, Genomes, and Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/30/2023
Publication Date: 6/20/2023
Citation: Minio, A., Ali, S., Cohen, S.P., Figueroa-Balderas, R., Carriel, D., Dahyana, B., Conrad Stack, J., Baruah, I., Jean-Philippe, M., Cantu, D., Bailey, B.A. 2023. Clonal Propagation of Moniliophthora roreri and the emergence of unique lineages with distinct genomes during range expansion. Genes, Genomes, and Genomics. https://doi.org/10.1093/g3journal/jkad125.
DOI: https://doi.org/10.1093/g3journal/jkad125

Interpretive Summary: Frosty pod rot of cacao, caused by the fungus Moniliophthora roreri, can greatly reduce cacao yields where it occurs in South and Central America. The pathogen specifically targets the fruit of cacao, the seeds of which are the source of chocolate, and causes severe yield losses. Although our understanding of how the pathogen causes disease is increasing, much of the genetic mechanisms controlling pathogen behavior remain unknown. We isolated DNA from multiple isolates of the fungus, using a collection of strains of the pathogen obtained throughout the areas where it occurs naturally. This DNA was used to assemble the pathogens genome and characterize unique aspects of its genome structure and gene composition. A pathogens genome and genetic makeup is a primary determinant in how the pathogen causes disease. Moniliophthora roreri does not sexually reproduce and as a result its genetic makeup is changing over time in unique ways depending on the area where specific isolates occur. As a result, plant breeders attempting to develop cultivars resistant to the pathogen can expect to find each growing area they choose to use for evaluating resistance to carry unique populations of the pathogen. As a result, it is important that new cultivars of cacao should be evaluated in multiple growing areas when screening for resistance to the pathogen Moniliophthora roreri.

Technical Abstract: The basidiomycete Moniliophthora roreri causes frosty pod rot of Theobroma cacao in the Western hemisphere. M. roreri is considered asexual and haploid throughout its hemibiotrophic lifecycle. To understand the processes driving genome modification, we sequenced and assembled five high quality M. roreri genomes out of a collection of ninety-nine isolates collected throughout the pathogen's range. We obtained chromosome-scale assemblies composed of 11 scaffolds. We also used short-read technology to sequence the genomes of twenty-two similarly chosen isolates. Alignments among the five reference assemblies revealed inversions and segmental translocations and duplications between and within scaffolds. Isolates at the front of the pathogens’ expanding range tend to share lineage-specific structural variants, as confirmed by short-read sequencing. We identified, for the first time, three new mating type A locus alleles (5 total) and one new potential mating type B locus allele (3 total). Currently only two mating type combinations, A1B1 and A2B2, are known to exist outside of Colombia. A systematic survey of the M. roreri transcriptome across twenty-two isolates identified an expanded candidate effector pool and provided evidence that effector candidate genes unique to the Moniliophthoras have been selected for preferential expression during the biotrophic phase of disease. Notably, M. roreri isolates in Costa Rica carry a chromosome segment duplication that has doubled the associated gene complement and includes secreted proteins and candidate effectors. Clonal propagation of the haploid M. roreri genome has allowed lineages with unique genome structures and compositions to dominate as it expands its range, displaying a significant founder effect.