Activation of HLS1 by Mechanical Stress via Ethylene-Stabilized EIN3 Is Crucial for Seedling Soil Emergence

Abstract

The seeds of terrestrial flowering plants often start their life cycle in subterranean darkness. To protect the fragile apical meristematic tissues and cotyledons from mechanical injuries during soil penetration, dicotyledonous seedlings form an elegant apical hook at the top of the hypocotyl. The apical hook has been considered as an adaption structure to the subterranean environment. However, the role of the apical hook in seedling emergence and the molecular mechanism of apical hook formation under real-life conditions remain highly speculative. Here, we find that HOOKLESS 1 (HLS1), a critical gene in apical hook formation in Arabidopsis thaliana, is required for seedling emergence from the soil. When grown under soil, hls1 mutant exhibits severe emergence defects. By contrast, HLS1 overexpression in the hls1 background fully restores emergence defects and displays better emergence capacity than that of WT. Our results indicate that HLS1 transcription is stimulated in response to the mechanical stress of soil cover, which is dependent on the function of the transcription factors ETHYLENE INSENSITIVE 3 (EIN3) and EIN3-LIKE 1 (EIL1). Soil-conferred mechanical stress activates the ethylene signaling pathway to stabilize EIN3 by repressing the activity of the F-box proteins EBF1 and EBF2. These combined results reveal a signaling pathway in which plant seedlings transduce the mechanical pressure of soil cover to correctly modulate apical hook formation during soil emergence.

On hormonal regulation of the dynamic apical hook development

“…These features of complexity might facilitate the adaptation of internal apical hook morphogenesis to the external soil condition. For instance, ethylene and jasmonic acid may integrate external factors, such as gaseous levels (Abbas et al ., ), soil compactness and mechanical stress (Chehab et al ., ; Shen et al ., ), gibberellin may coordinate the endogenous biological process from seed germination to the early hook formation process (Gallego‐Bartolome et al ., ), and auxin and cytokinin ultimately converge the signaling of other hormones to the control of cell expansion and division in the apical hook (Raz & Koornneef, ; Spartz et al ., ).…”

“…This transcriptional coupling integratively mediates the effects of multiple hormones, such as ethylene, gibberellin and jasmonate, and environmental factors, such as light and mechanical pressure, on apical hook development ( Fig. 1) (Gallego-Bartolome et al, 2011;An et al, 2012;Zhang et al, 2014Zhang et al, , 2018Jeong et al, 2016;Shen et al, 2016;Shi et al, 2018).…”

“…It has long been believed that dicotyledonous plants overcome this environmental challenge largely by the development of an arch-like structure, which is currently termed the apical hook, at the upper parts of the hypocotyl or epicotyl (Darwin & Darwin, 1881). The physiological significance of the proper development of the apical hook has been well documented in the model plant Arabidopsis (Harpham et al, 1991;Shen et al, 2016).…”

EIN3 and PIF3 Form an Interdependent Module That Represses Chloroplast Development in Buried Seedlings

“…For the chemical treatment, the seeds were plated on half-strength MS medium supplemented with 10 mM ACC, 100 mM AgNO 3 , or 25 mM AVG as previously described (An et al, 2010;Shen et al, 2016). The pER8:EIN3-Myc/ein3 eil1 and pER8:EIN3-Myc/pif3 ein3 eil1 seeds were plated on halfstrength MS medium containing 10 mM b-estradiol to induce EIN3-Myc expression.…”

“…As the essential transcription factor, EIN3 activates the expression of a wide range of downstream genes. Among these genes, ETHYLENE RESPONSE FACTOR (ERF1) is induced to slow hypocotyl elongation (Solano et al, 1998;Zhong et al, 2014), and HOOKLESS1 (HLS1) is activated to enhance apical hook formation (Lehman et al, 1996;Shen et al, 2016). Moreover, EIN3 inhibits Pchlide biosynthesis and directly activates the gene expression of both PROTOCHLOROPHYLLIDE OXIDOREDUCTASE A (PORA) and PORB in the cotyledon (Zhong et al, 2009(Zhong et al, , 2014.…”