The Stimulation of Indigenous Bacterial Antagonists by γ-Glutamyl--Allyl-l-Cysteine Increases Soil Suppressiveness to Fusarium Wilt.

The development of suppressive soil is an ideal strategy to sustainably combat soilborne diseases. Previously, the cultivation of Allium plants increased antagonistic bacteria populations in soil, alleviating Fusarium wilt of different crops. This study aimed to identify a compound produced by Allium plants that can induce bacteria-mediated soil suppressiveness toward Fusarium wilt. The amendment of soils with γ-glutamyl--allyl-l-cysteine (GSAC), a unique dipeptide abundantly detected in the root extract of Welsh onion (Allium fistulosum), significantly suppressed Fusarium wilt diseases, whereas three other commercial dipeptides had no such effects. GSAC application did not suppress the disease in sterilized soil. Furthermore, the suppressiveness of soil amended with GSAC could be transferred to sterilized soil via soil microflora transplantation. This suppressiveness was eliminated by pretreating GSAC-amended soil microflora with antibacterial antibiotics, indicating that the suppressiveness of GSAC-amended soil is generated by the activity of antagonistic bacteria. Amplicon sequencing of the 16S rRNA gene revealed that GSAC application significantly increased the relative abundance of Pseudomonas (OTU224), Burkholderia-Caballeronia-Paraburkholderia (OTU387), and Bdellovibrio (OTU1259) in soils. Surprisingly, the relative abundance of OTU224 was significantly greater in Welsh onion rhizospheres than in noncultivated soil. Pseudomonas strains corresponding to OTU224, isolated from Welsh onion rhizospheres, displayed a remarkable suppressive effect against cucumber Fusarium wilt, implying that OTU224 was involved in GSAC-mediated suppressiveness. This is the first study on the potential of GSAC as a soil microflora-manipulating agent that can enhance soil suppressiveness to Fusarium wilt. Methods for increasing soil suppressiveness via soil microflora manipulation have long been explored as an ideal strategy to protect plants from soilborne pathogens. However, viable methods offering consistent disease control effects have not yet been developed. Previously, the cultivation of Allium plants was demonstrated to induce bacteria-mediated soil suppressiveness to Fusarium wilt of different crop plants. This study discovered that the application of γ-glutamyl--allyl-l-cysteine, a unique dipeptide synthesized by Welsh onion, to soil enhances Fusarium wilt suppressiveness by increasing the relative abundance of indigenous antagonistic bacteria irrespective of the soil type. This finding will facilitate research supporting the development of environmentally friendly control measures for soilborne diseases.