Synthetic Polyploidisation Enhances Fusarium graminearum Tolerance in Wheat by Reshaping the Transcriptome and Strengthening the Microbiome.

Polyploidisation is a natural evolutionary mechanism that enhances plant stress tolerance and environmental adaptability; however, its impact on microbiome homeostasis remains poorly understood. In this study, we selected a nascent euploid synthetic hexaploid wheat line (HG116; 2n = 6x = 42, BBAADD) by selfing a triploid F1 hybrid of Triticum turgidum L. ssp. durum (Langdon, LDN; 2n = 4x = 28, BBAA) and Aegilops tauschii Coss. (SY41; 2n = 2x = 14, DD). We investigated the effects of synthetic polyploidisation on gene expression in roots, the root-associated microbiome and tolerance to Fusarium graminearum. Transcriptomic analysis revealed that polyploidisation in HG116 predominantly upregulated genes, which were enriched in stress- and defence-related pathways, particularly those involved in responses to pathogens and biotic stress. Microbiome profiling showed that HG116 recruited beneficial bacterial taxa and suppressed potential fungal pathogen growth in its rhizosphere and root endosphere compared to its parental lines. In F. graminearum inoculation experiments, HG116 demonstrated tolerance comparable to that of the F. graminearum-resistant variety, in contrast to its susceptible parental varieties. Moreover, HG116 maintained microbial homeostasis by enriching Gram-positive bacteria such as Actinobacteria and Firmicutes. F. graminearum inoculation also triggered extensive transcriptional reprogramming in HG116, including the upregulation of dehydrin, universal stress protein and defence-related genes, which might collectively contribute to F. graminearum tolerance. These findings support the possibility that synthetic polyploidisation could enhance wheat's tolerance to F. graminearum by reshaping transcriptomic and microbial networks, offering valuable insights for developing more resilient wheat cultivars.