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Title: Global distribution of mating types shows limited opportunities for mating across populations of fungi causing boxwood blight disease

Author
item Wight-Malapi, Martha
item VELTRI, DANIEL - Orise Fellow
item GEHESQUIÈRE, BJORN - Institute For Agricultural And Fisheries Research (ILVO)
item HEUNGENS, KURT - Institute For Agricultural And Fisheries Research (ILVO)
item RIVERA, YAZMIN - Rutgers University
item SALGADO-SALAZAR, CATALINA - Orise Fellow
item Crouch, Jo Anne

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/19/2019
Publication Date: 6/27/2019
Citation: Wight-Malapi, M., Veltri, D., Gehesquière, B., Heungens, K., Rivera, Y., Salgado-Salazar, C., Crouch, J. 2019. Global distribution of mating types shows limited opportunities for mating across populations of fungi causing boxwood blight disease. Fungal Genetics and Biology. https://doi.org/10.1016/j.fgb.2019.103246.
DOI: https://doi.org/10.1016/j.fgb.2019.103246

Interpretive Summary: Plant diseases brought about by fungi cause billions of dollars in losses to agricultural crops each year. Blight is a destructive new disease of boxwood plants that disfigures and eventually kills the infected plant. Two different species of fungi cause boxwood blight in Europe, but only a single fungus is present in the U.S., Asia, and New Zealand. In this research, we looked at blight fungi isolated from diseased boxwood plants from around the world to see whether they possess the genes needed to produce sexual offspring. To accomplish this work, we used a technology called next-generation sequencing to completely sequence the DNA of every gene from 16 different boxwood blight fungi. We used these DNA sequences to find the genes that serve as master regulators of mate recognition for fungi, and then used them to test these genes in 267 additional boxwood blight fungi collected from around the world. We identified the two required forms of the mating genes from the blight fungi, but found that each individual fungus only had one of the two forms. Our findings show that outside of Europe, sex is not possible for the boxwood blight fungi, and allows scientists to more easily predict their traits. This information and new tools will be useful for plant pathologists and breeders who are working to develop ways to control this disease. Plant quarantine personnel will use this research and the new diagnostic tools developed in this study to monitor these fungi and to keep the second European species from entering North America.

Technical Abstract: Boxwood blight is a disease threat to natural and managed landscapes worldwide. To determine mating potential of the fungi responsible for the disease, Calonectria pseudonaviculata and C. henricotiae, we characterized their mating-type (MAT) loci. Genome datasets were prepared from four Calonectria species and used to design PCR tests for mating-type from 268 isolates collected from four continents. Both fungal species have a MAT locus that is structurally consistent with the organization found in heterothallic ascomycetes, with just one idiomorph per individual isolate. Mating type was subdivided by species: all C. henricotiae isolates possessed the MAT1-1 idiomorph, whereas all C. pseudonaviculata isolates possessed the MAT1-2 idiomorph. To determine the potential for divergence at the MAT1 locus to present a barrier to interspecific hybridization, evolutionary analysis was conducted. Phylogenomic comparisons indicate that the two species diverged approximately 2.1 Mya. However, syntenic comparisons, phylogenetic trees, and estimates of nucleotide divergence across the MAT1 locus and proximal genes identified minimal nucleotide divergence between C. henricotiae and C. pseudonaviculata in this region of the genome. These results show that in North America and parts of Europe, where only C. pseudonaviculata resides, mating is constrained by the absence of MAT1-1, unless isolates can bypass the MAT self-sterility system. In regions of Europe where C. henricotiae and C. pseudonaviculata currently share the same host and geographic range, it remains to be determined whether or not these two recently diverged species are able to overcome species barriers to mate.