A mini-chromosome transcription factor CaGATA1 activates aldehyde dehydrogenase to regulate pathogenicity in Colletotrichum asianum.

Mini-chromosomes play pivotal roles in pathogenicity and host adaptation by filamentous plant pathogens, however the regulatory mechanisms underlying their virulence functions remain poorly understood. Here, we identified a novel GATA transcription factor, CaGATA1, encoded on the mini-chromosome of Colletotrichum asianum. CaGATA1 expression was markedly induced during infection. Functional analyses demonstrated that although CaGATA1 is dispensable for vegetative growth, it is essential for conidiation, appressorial formation, tolerance to oxidative stresses, and full virulence. Integrated RNA-seq and DAP-seq analyses revealed that CaGATA1 enables extensive transcriptional reprogramming by directly binding to conserved GATA-box motifs within the promoters of numerous virulence-associated genes. Among these targets, loss of CASFJ_03646 (encoding an aldehyde dehydrogenase, CaALDH1) in C. asianum impaired both fungal growth and pathogenicity. Yeast one-hybrid, EMSA, dual-luciferase assays, and structural modeling confirmed that CaGATA1 directly activates CaALDH1 transcription. The resulting elevation in ALDH activity facilitated the detoxification of reactive aldehydes, thereby sustaining fungal development and infection capacity. Collectively, our findings uncover a regulatory pathway through which mini-chromosome-encoded CaGATA1 regulates CaALDH1 to promote oxidative stress adaptation and pathogenicity in C. asianum, providing potential targets for the management of anthracnose.