WC1/WC2-Sre1 Transcriptional Cascade Controls Predation and Chlamydospore Formation in the Nematode-Trapping Fungus Arthrobotrys flagrans.

Arthrobotrys flagrans is a nematode-trapping fungus that kills plant-parasitic nematodes (PPNs) using adhesive traps and withstands adverse conditions by producing chlamydospores. It holds promise as a biocontrol agent against PPNs, yet the mechanisms underlying its pathogenicity and chlamydospore formation remain poorly characterized, hampering the development of efficient biocontrol strains. Here, we systematically characterized all eight GATA-type transcription factors in A. flagrans and found that all were significantly upregulated during both trap and chlamydospore formation. These eight regulators exhibit specialized and coordinated functions in hyphal growth, stress responses, pathogenicity, and chlamydospore formation. WC2, WC1, Sre1, AreA, ASD4 and GATA1 positively regulate pathogenicity, whereas Ams2 and NsdD act as negative regulators, likely through the repression of virulence factors and adhesins. Moreover, all eight factors govern chlamydospore number, with WC1, WC2 and Sre1 additionally controlling chlamydospore diameter. Further investigation of their interactions and regulatory relationships revealed a novel, light-independent WC1/WC2-Sre1 transcriptional cascade as a key node within the network governing pathogenicity and chlamydospore formation. Overexpression of WC2 significantly increases pathogenicity and chlamydospore production, providing functional validation that WC2 is a precise genetic target for engineering superior biocontrol strains. Overall, this work elucidates the functional atlas of GATA-type transcription factors in A. flagrans, reveals a novel light-signalling co-option mechanism for developmental regulation, and provides both actionable molecular targets for strain improvement and a theoretical framework for advancing the biocontrol of PPNs.