Macrophomina phaseolina clonal and recombinant genotypes specialize for virulence on strawberry and soybean

Authors: PENNERMAN, KAYLA - Oak Ridge Institute For Science And Education (ORISE); Goldman, Polly; DILLA-ERMITA, JADE - University Of California; Ramos, Gerardo; AVILES, MANUEL - University Of Seville; BORRERO, CELIA - University Of Seville; GOMEZ, APOLLO - Queensland Government; NEAL, JODI - Queensland Government; CHILVERS, MARTIN - Michigan State University; ORTIZLONDONO, VIVIANA - Michigan State University; STUKENBROCK, EVA - University Of Kiel; GOLDMAN, GUSTAVO - Universidade De Sao Paulo; Mengistu, Alemu; SEIJO, TERESA - University Of Florida; PEREZ, NATALIA - University Of Florida; BROOME, JENNY - Driscolls; IVORS, KELLY - Driscolls; COLE, GLENN - University Of California; KNAPP, STEVE - University Of California; MCFARLANE, DYLAN - Victorian Strawberry Industry Development Committee; MATTNER, SCOTT - Victorian Strawberry Industry Development Committee; GAMBARDELLA, MARINA - Catholic Pontifical University Of Chile; Henry, Peter

Submitted to: Fungal Genetics Conference
Publication Type: Abstract Only
Publication Acceptance Date: 12/2/2023
Publication Date: 3/12/2024
Citation: Pennerman, K.K., Goldman, P.H., Dilla-Ermita, J., Ramos, G., Aviles, M., Borrero, C., Gomez, A., Neal, J., Chilvers, M., Ortizlondono, V., Stukenbrock, E.H., Goldman, G.H., Mengistu, A., Seijo, T., Perez, N., Broome, J., Ivors, K., Cole, G., Knapp, S., Mcfarlane, D., Mattner, S., Gambardella, M., Henry, P.M. 2024. Macrophomina phaseolina clonal and recombinant genotypes specialize for virulence on strawberry and soybean. Fungal Genetics Conference, March 12-17, 2024, Pacific Grove, California.

Interpretive Summary:

Technical Abstract: Macrophomina phaseolina has a broad host range, but individual isolates may be pathogenic to a limited number of hosts as previous work has shown. However, a comprehensive understanding of host susceptibility by pathogen genotype interactions is lacking. There is also incomplete knowledge of how Macrophomina spp. genetic diversity is generated and maintained. Information about host specificity and the potential for recombination would be instrumental to future control efforts of the fungus. A survey of Macrophomina spp. was conducted to identify host ' pathogen genotype associations, pangenomic structure and mechanisms of genetic exchange. Short-read sequence data were obtained for 427 Macrophomina spp. isolates collected from 92 host plant species and soil in 23 countries. High-quality SNPs identified with three genomic references grouped M. phaseolina into eight lineage clusters, with high admixture in some isolates and equal mating type ratios in some clusters suggesting on-going meiotic recombination. Three of the identified clusters were associated with the isolates’ host of origin; 82% of strawberry-derived isolates were in a single clonal lineage, whereas 89% of soybean isolates resolved into two admixed lineages. This pattern suggested that host specialization may have occurred among isolates in specific clusters. Pathogenicity tests of select isolates from each cluster showed only isolates from the strawberry-associated cluster were highly aggressive against the host. Isolates from other clusters did not yield disease symptoms. However, we did not find genes or genomic regions that were exclusive and universal to strawberry cluster isolates, suggesting that strawberry specialization within M. phaseolina is governed by polygenes, gene regulation and/or epigenetic effects. The SNP and gene sequence data grouped three Macrophomina spp. into two clusters that were distinct from M. phaseolina. Two of these species, M. euphorbiicola and M. pseudophaseolina, had fewer SNP and genetic differences between them than did clusters of M. phaseolina isolates. This suggests that M. euphorbiicola and M. pseudophaseolina should be considered a single species. Our work provides insight into host specialization and evolutionary mechanisms within this economically-important phytopathogenic genus.