Hijacking the Host Clock: A Nematode Effector Antagonizes Soybean Circadian Defense and Translation Control

ABSTRACT The majority of commercially cultivated soybean cyst nematode (SCN)‐resistant soybean cultivars rely on the Rhg1 locus to defend against SCN, the most economically destructive soybean root pathogen. The decline of Rhg1's effectiveness due to its continuous use creates an urgent need for alternative genetic sources to sustain SCN resistance. Although pathogen effectors are known to perturb host circadian clocks in other plant‐pathogen systems, whether and how plant‐parasitic nematodes interfere with the host clock to promote virulence remains unexplored. Here, we report that the soybean circadian clock gates rhythmic defense against SCN, and its core component, GmCCA1, plays a dual role in both circadian regulation and pathogen defense. Surprisingly, overexpression of GmCCA1 disrupts circadian rhythms but confers sustained resistance against SCN by activating defense genes both within and beyond the Rhg1 locus, including various pathogenesis‐related and resistance genes. On the pathogen side, we identify Hg4E02—an evolutionarily conserved effector in plant‐parasitic nematodes—as a transcriptional regulator that directly binds to the promoters of multiple clock genes via novel cis‐elements, suppressing their expression. Hg4E02 also represses defense gene expression to enhance virulence. Notably, we uncover a previously unknown layer of antagonism: GmCCA1 and Hg4E02 exert opposing effects on both defense genes and translation‐related genes. GmCCA1 inhibits translation and root growth, whereas Hg4E02 promotes translation, likely facilitating nutrient acquisition for the nematode. Collectively, our study reveals a novel mechanism by which a nematode effector directly targets the host circadian clock and translation machinery to promote parasitism, and proposes GmCCA1 as a promising engineering target for enhancing SCN resistance in soybean.