Ethylene-orchestrated circuitry coordinates a seedling's response to soil cover and etiolated growth

The early life of terrestrial seed plants often starts under the soil in subterranean darkness. Over time and through adaptation, plants have evolved an elaborate etiolation process that enables seedlings to emerge from soil and acquire autotrophic ability. This process, however, requires seedlings to be able to sense the soil condition and relay this information accordingly to modulate both the seedlings' growth and the formation of photosynthetic apparatus. The mechanism by which soil overlay drives morphogenetic changes in plants, however, remains poorly understood, particularly with regard to the means by which the cellular processes of different organs are coordinated in response to disparate soil conditions. Here, we illustrate that the soil overlay quantitatively activates seedlings' ethylene production, and an EIN3/EIN3-like 1-dependent ethylene-response cascade is required for seedlings to successfully emerge from the soil. Under soil, an ERF1 pathway is activated in the hypocotyl to slow down cell elongation, whereas a PIF3 pathway is activated in the cotyledon to control the preassembly of photosynthetic machinery. Moreover, this latter PIF3 pathway appears to be coupled to the ERF1-regulated upward-growth rate. The coupling of these two pathways facilitates the synchronized progression of etioplast maturation and hypocotyl growth, which, in turn, ultimately enables seedlings to maintain the amount of protochlorophyllide required for rapid acquisition of photoautotrophic capacity without suffering from photooxidative damage during the dark-to-light transition. Our findings illustrate the existence of a genetic signaling pathway driving soil-induced plant morphogenesis and define the specific role of ethylene in orchestrating organ-specific soil responses in Arabidopsis seedlings.