Transmission, localization, and infectivity of seedborne maize chlorotic mottle virus

Authors: BERNARDO, PAULINE - The Ohio State University; Barriball, Kelly; FREY, TIMOTHY - The Ohio State University; MEULIA, TEA - The Ohio State University; WANGAI, ANNE - Kenya Agricultural And Livestock Research Organization; SURESH, L - International Maize & Wheat Improvement Center (CIMMYT); HEUCHELIN, SCOTT - Corteva Agriscience; PAUL, PIERCE - The Ohio State University; Redinbaugh, Margaret; Ohlson, Erik

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/27/2023
Publication Date: 2/6/2023
Citation: Bernardo, P., Barriball, K., Frey, T.S., Meulia, T., Wangai, A., Suresh, L., Heuchelin, S., Paul, P., Redinbaugh, M.G., Ohlson, E.W. 2023. Transmission, localization, and infectivity of seedborne maize chlorotic mottle virus. PLOS ONE. 18(2). Article #e0281484. https://doi.org/10.1371/journal.pone.0281484.
DOI: https://doi.org/10.1371/journal.pone.0281484

Interpretive Summary: Maize lethal necrosis (MLN) is a highly destructive disease that occurs when corn is infected by maize chlorotic mottle virus (MCMV) in combination with a secondary virus, most commonly sugarcane mosaic virus (SCMV). Since SCMV is widespread globally, outbreaks of MLN are typically associated with the introduction of MCMV, possibly through seed. Understanding the frequency and mechanisms of seedborne MCMV transmission is critical for developing effective management strategies. In this study, more than 85,000 corn seedlings were grown and evaluated for the presence of MCMV to determine transmission frequency and localization of MCMV in the seed was determined. Transmission frequency was found to be less than 0.01%, indicating that seedborne transmission of MCMV is highly inefficient. MCMV was only detected on maternal seed tissues, that are incapable of sustaining living virus since they dry and become dead tissues during seed maturation, and never detected in the living embryonic tissue, the tissue that develops into the seedling. These findings suggest that seedborne transmission of MCMV is minimal and unlikely to be a significant factor in countries where MCMV is already present. However, low seedborne transmission rates were detected, especially among seed with higher moisture content, suggesting that MCMV can still be spread through seed trade to areas where the disease is not present. A better understanding of the mechanisms influencing seedborne transmission of MCMV will help seed companies develop improved seed treatments and reduce the spread of MCMV through seed, benefiting growers.

Technical Abstract: Maize lethal necrosis is a destructive synergistic virus disease of maize caused by maize chlorotic mottle virus (MCMV) in combination with a virus in the family Potyviridae. Emergence of MLN is typically associated with the introduction of MCMV or its vectors and understanding its spread through seed is critical for disease management. Previous studies suggest that the rate of MCMV transmission through seed is low, despite detection of the virus on seed. However, mechanisms influencing its transmission are poorly understood. Elucidating these mechanisms is crucial for informing strategies to prevent spread on contaminated seed. In this study, we evaluated the rate of MCMV seed transmission using seed collected from plants that were artificially inoculated with MCMV isolates from Hawaii and Kenya. Grow-out tests indicated that MCMV transmission through seed was rare, with a rate of 0.01% among the more than 85,000 seed evaluated, despite detection of MCMV at high levels in the seed lots. To understand factors that limit transmission from seed, MCMV distribution in seed tissues was examined using serology and immunolocalization. The virus was present at high levels in maternal tissues, the pericarp and pedicel, but absent from filial endosperm and embryo tissues. The ability to transmit MCMV from seed to uninfected plants was tested to evaluate virus viability. Transmission was negatively associated with both seed maturity and moisture content. Transmission of MCMV from infested seed dried to less than 15% moisture was not detected, suggesting proper handling could be important for minimizing spread of MCMV through seed.