Uncovering the Infection Strategy of Phyllachora maydis during Maize Colonization: A Comprehensive Analysis

Authors: CALDWELL, DENISE - Purdue University; DA SILVA, CAMILA - Purdue University; MCCOY, AUSTIN - Michigan State University; AVILA, HARRYSON - Purdue University; BONKOWSKI, JOHN - Purdue University; CHILVERS, MARTIN - Michigan State University; Helm, Matthew; TELENKO, DARCY - Purdue University; IYER-PASCUZZI, ANJALI - Purdue University

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/6/2023
Publication Date: 5/31/2024
Citation: Caldwell, D., Da Silva, C., McCoy, A., Avila, H., Bonkowski, J., Chilvers, M., Helm, M.D., Telenko, D., Iyer-Pascuzzi, A. 2024. Uncovering the Infection Strategy of Phyllachora maydis during Maize Colonization: A Comprehensive Analysis. Phytopathology. https://doi.org/10.1094/PHYTO-08-23-0298-KC.
DOI: https://doi.org/10.1094/PHYTO-08-23-0298-KC

Interpretive Summary: Plant diseases caused by fungal plant pathogens are among the most severe limiting factors in global crop production. Such diseases cause an estimated 10-20% yield loss worldwide annually, with an additional 10%-20% loss post-harvest. Phyllachora maydis is fungal pathogen that causes tar spot disease, a foliar disease of maize (corn) commonly found with in the United States. Tar spot was first detected in the U.S. in 2015 and has caused an estimated $2.9 billion yield loss to U.S. farmers. Despite the importance of tar spot disease to U.S. farmers, very little is known how this fungal pathogen invades and colonizes maize leaf tissue. Using advanced microscopy methods, we show this fungal pathogen first penetrates through the outermost cell layer of the maize leaf tissue (i.e. epidermis) and then subsequently forms reproductive structures below the epidermis. Once the reproductive structures are formed, P. maydis produces spores that are then discharged from the host cell tissues and function to propagate further infection and disease of the host. Unlike other plant pathogens, we show P. maydis does not colonize the vasculature tissue of maize, suggesting this fungal pathogen does not spread using the vasculature system. This study is the first to investigate how this fungal pathogen colonizes and spreads within maize, and sheds lights on how P. maydis causes disease. This knowledge will likely help to development new approaches for managing this disease for U.S. farmers.

Technical Abstract: Tar spot, a disease caused by the ascomycete fungal pathogen Phyllachora maydis, is considered one of the most significant yield-limiting diseases of maize (Zea mays L.) within the United States, responsible for twice as much yield loss as any other fungal pathogen in 2022. P. maydis may be found in association with other fungi, forming a disease complex with characteristic fish eye lesions. Understanding how P. maydis invades and colonizes maize leaf cells is essential for developing effective disease control strategies. Here, we used histological approaches to elucidate how P. maydis infects and multiplies within susceptible maize leaves. We collected tar spot-infected maize leaf samples from four different fields in northern Indiana at three different time points during the growing season. Samples were chemically fixed and paraffin-embedded for high-resolution light and scanning electron microscopy. We observed a consistent pattern of disease progression in independent leaf samples collected across different geographical regions. Each stromata contained a central pycnidium that produced asexual spores and fungal hyphae colonized epidermal cells that became melanized, forming a clypeus-like structure. Perithecia with sexual spores developed in the stomatal chambers adjacent to the pycnidia, and a cap of spores formed over the stromata. P. maydis reproductive structures formed around but not within the vasculature. In our fish eye samples, P. maydis is associated with two additional fungi, one of which is likely a member of the Paraphaeospheria genus; the other is an unknown fungi. Our data provide fundamental insights into how this fungal pathogen colonizes and spreads within maize leaves and sheds light on disease progression within a leaf. This knowledge can inform the development of new approaches to managing tar spot, which could help mitigate the significant economic losses caused by this disease.