Phyllachora species infecting maize and other grass species in the Americas represents a complex of closely related species

Authors: Broders, Kirk; IRIARTE-BRODERS, GLORIA - Collaborator; BERGSTROM, GARY - Cornell University; BYAMUKAMA, EMMANUEL - South Dakota State University; CHILVERS, MARTIN - Michigan State University; CRUZ, CHRISTIAN - Purdue University; DALLA-LANA, FELIPE - Pennsylvania State University; DURAY, ZACHARY - University Of Illinois; MALVICK, DEAN - University Of Minnesota; MUELLER, DAREN - Iowa State University; PAUL, PIERCE - The Ohio State University; PLEWA, DIANE - University Of Illinois; RAID, RICHARD - University Of Florida; ROBERTSON, ALISON - Iowa State University; Salgado-Salazar, Catalina; SMITH, DAMON - University Of Wisconsin; TELENKO, DARCY - Pennsylvania State University; VANETTEN, KATHERINE - University Of Illinois; KLECZEWSKI, NATHAN - University Of Illinois

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/31/2022
Publication Date: 4/25/2022
Citation: Broders, K., Iriarte-Broders, G., Bergstrom, G.C., Byamukama, E., Chilvers, M., Cruz, C., Dalla-Lana, F., Duray, Z., Malvick, D., Mueller, D., Paul, P., Plewa, D., Raid, R., Robertson, A.E., Salgado, C., Smith, D., Telenko, D., VanEtten, K., Kleczewski, N.M. 2022. Phyllachora species infecting maize and other grass species in the Americas represents a complex of closely related species. Ecology and Evolution. 12(4): Article e8832. https://doi.org/10.1002/ece3.8832.
DOI: https://doi.org/10.1002/ece3.8832

Interpretive Summary: The fungal pathogen Phyllachora maydis causes the disease tar spot on corn, which has recently emerged as a major threat to corn production throughout North America. The origin of this disease is still unclear, and there may potentially be more than one species of this pathogen causing the disease. An ARS researcher at Peoria, Il, collaborated with researchers at the University of Illinois and several other universities in the U.S. to sample tar spot disease from across South, Central and North America to understand the origin and diversity of the pathogen causing tar spot disease. Analyses of DNA data determined there are 3 species of Phyllachora that cause tar spot of corn in the U.S. It is likely these three species originated in Mexico, Central America, and the Caribbean. These results indicate the fungus is native to North America and the emergence of the disease is likely due to a change in climate making the corn growing region of the U.S. more hospitable for the fungus and a shift in corn genetics that resulted in a lack of resistance to the three Phyllachora species that cause this disease. These results will be of interest to corn breeders, pathologists, agronomists and corn growers as the try to better understand the biology of this fungus and develop resistant varieties and crop management strategies to reduce yield loss due to this disease.

Technical Abstract: The genus Phyllachora contains numerous obligate fungal parasites that produce raised, melanized structures called stromata on their plant hosts referred to as tar spot. Members of this genus are known to infect many grass species but generally do not cause significant damage or defoliation, with the exception of P. maydis which has emerged as an important pathogen of maize throughout the Americas, but the origin of this pathogen remains unknown. To date, species designations for Phyllachora have been based on host associations and morphology, and most species are assumed to be host specific. We assessed the sequence diversity of 186 single stroma isolates collected from 16 hosts representing 15 countries. Samples included both herbarium and contemporary strains that covered a temporal range from 1905 to 2019. These 186 isolates were grouped into five distinct species with strong bootstrap support. We found three closely related, but genetically distinct groups of Phyllachora are capable of infecting maize in the United States, we refer to these as the P. maydis species complex. Based on herbarium specimens, we hypothesize that these three groups in the P. maydis species complex originated from Central America, Mexico, and the Caribbean. Although two of these groups were only found on maize, the third and largest group contained contemporary strains found on maize and other grass hosts, as well as herbarium specimens from maize and other grasses that include 10 species of Phyllachora. The herbarium specimens were previously identified based on morphology and host association. This work represents the first attempt at molecular characterization of Phyllachora species infecting grass hosts and indicates some Phyllachora species can infect a broad range of host species and there may be significant synonymy in the Phyllachora genus.