Iron-Flavonoid-Peroxidase Signaling Triggers Seed-Coat Remodeling for Rapid Germination

Seed germination and survival depend on a sustained water supply. The mechanisms by which seeds determine how much water is available remain elusive. We previously observed that iron (Fe) supply accelerates germination in tomato. Using Arabidopsis thaliana, we show here that increased Fe in the spermosphere during flood acts as an extrinsic signal that increases seed coat permeability. Fe triggers structural remodeling of the cuticle covering the endosperm, as evidenced by loss of Auramine O staining in the testa-ruptured seeds. Fe-triggered germination phenotypes are compromised in the flavonoid (tt4 and tt7) and prx17 mutants, and in peroxidase inhibitor-treated wild-type plants. We hypothesize that PRX17-driven peroxidase activity is governed by a maternal repressor-derepressor mechanism in which seed coat flavonoids constitutively repress enzyme activity. This repression is relieved by chelation of Fe by flavonoids, allowing PRX17 to remodel the cuticle and accelerate germination. To test this model, we examined the interaction between Fe and peroxidases with quercetin, a major seed coat flavonoid. Upon imbibition, quercetin is deglycosylated and inhibits PRX17 activity. Formation of Fe-quercetin complexes at the chalaza reduces the level of active quercetin, thereby restoring PRX17 activity in a dose-dependent manner. This study reveals that elevated Fe levels in oxygen-deprived, submerged soils prime seeds for rapid germination, a novel control mechanism mediated by seed coat biochemistry.