Light‐induced stabilization of ACS contributes to hypocotyl elongation during the dark‐to‐light transition in Arabidopsis seedlings

Abstract

Summary Hypocotyl growth during seedling emergence is a crucial developmental transition influenced by light and phytohormones such as ethylene. Ethylene and light antagonistically control hypocotyl growth in either continuous light or darkness. However, how ethylene and light regulate hypocotyl growth, including seedling emergence, during the dark‐to‐light transition remains elusive. Here, we show that ethylene and light cooperatively stimulate a transient increase in hypocotyl growth during the dark‐to‐light transition via the light‐mediated stabilization of 1‐aminocyclopropane‐1‐carboxylic acid (ACC) synthases (ACSs), the rate‐limiting enzymes in ethylene biosynthesis. We found that, in contrast to the known inhibitory role of light in hypocotyl growth, light treatment transiently increases hypocotyl growth in wild‐type etiolated seedlings. Moreover, ACC, the direct precursor of ethylene, accentuates the effects of light on hypocotyl elongation during the dark‐to‐light transition. We determined that light leads to the transient elongation of hypocotyls by stabilizing the ACS5 protein during the dark‐to‐light transition. Furthermore, biochemical analysis of an ACS5 mutant protein bearing an alteration in the C‐terminus indicated that light stabilizes ACS5 by inhibiting the degradation mechanism that acts through the C‐terminus of ACS5. Our study reveals that plants regulate hypocotyl elongation during seedling establishment by coordinating light‐induced ethylene biosynthesis at the post‐translational level. Moreover, the stimulatory role of light on hypocotyl growth during the dark‐to‐light transition provides additional insights into the known inhibitory role of light in hypocotyl development.

Ethylene signaling in plants

“…However, environmental factors such as dark versus light or the presence of other hormones can affect this so that depending on conditions, EIN3 interacts with other transcription factors leading to outputs not predicted by the common ethylene signaling models (179)(180)(181). As an example, ethylene is well known for inhibiting hypocotyl growth in dark-grown eudicot seedlings (36,182) and stimulating hypocotyl growth in the light (183)(184)(185)(186)(187). In the dark, EIN3 directly interacts with another transcription factor, phytochrome interacting factor3 (PIF3), forming an output module distinct from either transcription factor alone (181).…”

Light Modulates Ethylene Synthesis, Signaling, and Downstream Transcriptional Networks to Control Plant Development

“…Light inhibits hypocotyl elongation, which is important as plants growing in soil transition to light (Montgomery, 2016). In opposition to the effect of ethylene in the dark, light-grown Arabidopsis seedlings show increased hypocotyl elongation in response to ethylene (Smalle et al, 1997; Le et al, 2005; Das et al, 2016; Seo and Yoon, 2019), as illustrated in Figure 1 . In both light and dark, the ACC or ethylene response is tied to differences in cell expansion (Smalle et al, 1997; Seo and Yoon, 2019).…”

“…In opposition to the effect of ethylene in the dark, light-grown Arabidopsis seedlings show increased hypocotyl elongation in response to ethylene (Smalle et al, 1997; Le et al, 2005; Das et al, 2016; Seo and Yoon, 2019), as illustrated in Figure 1 . In both light and dark, the ACC or ethylene response is tied to differences in cell expansion (Smalle et al, 1997; Seo and Yoon, 2019). These light-dependent differences have more frequently been reported in response to treatment with the ethylene precursor, ACC (Smalle et al, 1997; Le et al, 2005), but ethylene yields the same light-dependent increases in elongation ( Figure 1 ), and ethylene-insensitive mutants are shorter than wild-type in the light (Le et al, 2005).…”

1-Aminocyclopropane 1-Carboxylic Acid and Its Emerging Role as an Ethylene-Independent Growth Regulator

“…Moreover, the heterodimerization with ACS7 increased the stability of both ACS2 and ACS5 as compared to the respective homodimers, which suggests that dimerization among various ACS isoforms may regulate their turnover rate and, as a result, ethylene biosynthesis (Lee et al, 2017). ACS5 proteins are also stabilized when etiolated Arabidopsis seedlings are moved to the light, promoting ethylene biosynthesis and hypocotyl elongation during this transition (Seo and Yoon, 2019).…”