Water-soluble exudates from seeds of Kochia scoparia exhibit antifungal activity against Colletotrichum graminicola

Authors: HOULIHAN, ADAM - RANDOLPH COLLEGE; CONLIN, PETER - UNIVERSITY OF ILLINOIS; Chee Sanford, Joanne

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/25/2019
Publication Date: 6/19/2019
Citation: Houlihan, A.J., Conlin, P., Chee-Sanford, J.C. 2019. Water-soluble exudates from seeds of Kochia scoparia exhibit antifungal activity against Colletotrichum graminicola. PLoS One. 14(6):e0218104. https://doi.org/10.1371/journal.pone.0218104.
DOI: https://doi.org/10.1371/journal.pone.0218104

Interpretive Summary: Plants employ a variety of strategies to resist disease caused by microbial infection. Seeds of weedy plant species were found to exude chemicals that include antimicrobial compounds. Water-soluble seed exudates from 14 weed species were tested for antagonistic activity against 16 fungal and 9 bacterial phytopathogens. Of the plant species tested, including members of the Asteraceae, Polygonaceae, Malvaceae, Convolvulaceae, Chenopodiaceae and Poaceae families, only kochia (Kochia scoparia) and jimsonweed (Datura stramonium) had detectable antimicrobial activity. Both kochia and jimsonweed are summer annual weeds that are common to the midwest agricultural region. Kochia exudates inhibited Colletotrichum graminicola, a pathogenic fungus that causes maize anthracnose and Taphrina deformans, a fungus that causes fruit tree leaf curl. Jimsonweed repressed Clavibacter michiganensis ssp. nebraskense, a significant phytobacterium that causes disease in tomatoes and potatoes. In all cases, the minimum inhibitory concentration was 3.125 mg of seed exudate dry mass per liter. The significance of this study shows that natural compounds produced by plants, including common weed species, have antimicrobial activities that may have useful properties for controlling crop pathogenic fungi and bacteria.

Technical Abstract: Plant seed exudates are composed of complex mixtures of chemicals with potential for bioactive compounds with antimicrobial properties. This study focused on kochia (Kochia scoparia), one of many weedy plant species considered invasive in many agricultural systems. Extraction of compounds in water yielded an exudate mass equivalent to 7% of the original seed mass used. Water-soluble exudates were tested against 16 known plant pathogens in disk diffusion assays and kochia exudates were found to inhibit Colletotrichum graminicola, the fungal causative agent of anthracnose and stalk rot in maize. The narrow range of fungi found as targets suggested the mechanism of inhibition may be specific rather than broadly antifungal. A decline in viability of cells over four orders of magnitude occurred within six hours of exposure to exudate. The minimum inhibitory concentration was 3.125 mg L-1. Hyphae formation in C. graminicola appeared inhibited following exposure to the exudate. Small molecular weight compounds as determined by GC/MS analysis showed high relative amounts of the sugars fructose, galactopyranose, glucose, and sorbitol, along with moderate proportions of organic acids and amino acids. Protein content averaged 0.7% in the standard concentration (100 mg mL-1) used for inhibition assays. Size fractionation of the exudate and subsequent disk diffusion assays revealed bioactive fractions with compounds in the MW range <5 kDa. To the best of our knowledge, this study is the first to show promising bioactivity against C. graminicola that was associated with water-extractable compounds from a common weed species. The results suggest that seeds of persistent plant species with long-lived seed banks like kochia may have potential for use in the discovery of compounds active in inhibiting fungal pathogens.