BBX32 integrates ethylene and light signaling to delay apical hook opening and optimize seedling soil emergence

Abstract

In terrestrial plants, seeds often germinate and initiate early development in the darkness under layers of soil. Soil overlay promotes ethylene accumulation to maintain the hook until the seedlings reach the soil surface. During this phase of etiolated growth and soil emergence, seedlings perceive changing light fluence. Coordinated interplay of the ethylene and light signaling pathways ensures optimal timing of apical hook opening and enhanced emergence. Here, we report that ethylene and light cooperatively act on the B-box protein BBX32 to regulate apical hook opening and enhance soil emergence. Ethylene induces expression and accumulation of BBX32 in the apical hook in the dark. CONSTITUTIVE PHOTOMORPHOGENIC 1 degrades BBX32 in the dark while light enhances BBX32 expression and accumulation in the apical hook during de-etiolation. bbx32 mutants exhibit accelerated apical hook opening, while BBX32 overexpressing lines show delayed opening. Genetic analyses reveal that BBX32 functions in concert with PHYTOCHROME-INTERACTING FACTOR 3 to negatively regulate apical hook opening during de-etiolation. BBX32 enhances HOOKLESS 1 expression in a PIF3-dependent manner to delay hook opening. Under soil cover, bbx32 and 35S:BBX32 seedlings exhibit reduced and enhanced seedling emergence, respectively. Our study illustrates the role of BBX32 in synchronizing light and ethylene-mediated apical hook opening and seedling emergence.