Interactive transcriptome analyses of Northern Wild Rice (Zizania palustris L.) and Bipolaris oryzae show convoluted communications during the early stages of fungal brown spot development

Authors: CASTELL-MILLER, CLAUDIA - University Of Minnesota; KONO, TOM - University Of Minnesota; RANJAN, ASHISH - University Of Minnesota; Schlatter, Daniel; Samac, Deborah - Debby; KIMBALL, JENNIFER - University Of Minnesota

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/22/2024
Publication Date: 4/26/2024
Citation: Castell-Miller, C.V., Kono, T., Ranjan, A., Schlatter, D.C., Samac, D.A., Kimball, J.A. 2024. Interactive transcriptome analyses of Northern Wild Rice (Zizania palustris L.) and Bipolaris oryzae show convoluted communications during the early stages of fungal brown spot development. Frontiers in Plant Science. 15. Article number 1350281. https://doi.org/10.3389/fpls.2024.1350281.

Interpretive Summary: Minnesota is the major producer of cultivated wild rice in the United States. However, fungal diseases, particularly fungal brown spot, are major threats to grain production. Genetic resistance to the disease is scarce, so farmers rely on fungicides of crop protection. There is a gap in knowledge of the genes expressed in the plant in response to infection, which hampers development of resistant cultivars. We also lack knowledge of the genes used by the fungal brown spot pathogen to cause disease. This experiment identified the plant and fungal genes expressed during the first 48 hours of plant-fungal interactions. The fungus produced enzymes for degrading plant cell walls and proteins to defeat plant defenses. The wild rice plants produced numerous defensive enzymes and antimicrobial compounds, some of which are unique to wild rice and not found in other grain crops. These genes can guide selection of plants for boosting defenses and help to develop more efficient selection of plants through use of the most virulent fungal isolates. Improved plant cultivars will reduce the economic and environmental costs of wild rice production through a reduced reliance on fungicides and help to maintain a stable and competitive provision of wild rice to markets.

Technical Abstract: Fungal diseases, mostly caused by Bipolaris spp., are past and current threats to Northern Wild Rice (NWR) grain production and germplasm preservation in both natural and cultivated settings. Genetic resistance against the pathogen is scarce. Toward expanding our understanding of the global gene communications of NWR and B. oryzae interactions, we designed an RNAseq study encompassing the first 12 h and 48 h of their encounter. NWR activated numerous plant recognition receptors after pathogen infection, followed by active transcriptional reprogramming of signaling mechanisms driven by Ca+2 and its sensors, mitogen-activated protein kinase cascades, activation of an oxidative burst, as well as phytohormone signaling bound-mechanisms. Several transcription factors associated with plant defense were found to be expressed. Importantly, evidence of diterpenoid phytoalexins, especially phytocassane biosynthesis, among expression of other defense genes was found. In B. oryzae, predicted genes associated with pathogenicity including secreted effectors that could target plant defense mechanisms were expressed. This study uncovered the early molecular communication between the NWR-B. oryzae pathosystem that could guide selection for allele-specific genes to boost NWR defenses and help to develop more efficient selection of plants in NWR breeding through the use of the most virulent fungal isolates.