Ethylene Promotes Hypocotyl Growth and HY5 Degradation by Enhancing the Movement of COP1 to the Nucleus in the Light

Abstract

In the dark, etiolated seedlings display a long hypocotyl, the growth of which is rapidly inhibited when the seedlings are exposed to light. In contrast, the phytohormone ethylene prevents hypocotyl elongation in the dark but enhances its growth in the light. However, the mechanism by which light and ethylene signalling oppositely affect this process at the protein level is unclear. Here, we report that ethylene enhances the movement of CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1) to the nucleus where it mediates the degradation of LONG HYPOCOTYL 5 (HY5), contributing to hypocotyl growth in the light. Our results indicate that HY5 is required for ethylene-promoted hypocotyl growth in the light, but not in the dark. Using genetic and biochemical analyses, we found that HY5 functions downstream of ETHYLENE INSENSITIVE 3 (EIN3) for ethylene-promoted hypocotyl growth. Furthermore, the upstream regulation of HY5 stability by ethylene is COP1-dependent, and COP1 is genetically located downstream of EIN3, indicating that the COP1-HY5 complex integrates light and ethylene signalling downstream of EIN3. Importantly, the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) enriched the nuclear localisation of COP1; however, this effect was dependent on EIN3 only in the presence of light, strongly suggesting that ethylene promotes the effects of light on the movement of COP1 from the cytoplasm to the nucleus. Thus, our investigation demonstrates that the COP1-HY5 complex is a novel integrator that plays an essential role in ethylene-promoted hypocotyl growth in the light.

Salt Stress and Ethylene Antagonistically Regulate Nucleocytoplasmic Partitioning of COP1 to Control Seed Germination

“…In the dark, COP1 is mainly located in the nucleus, mediating the degradation of its target proteins, such as HY5. However, light can inhibit this activity by reducing the nuclear abundance of COP1 and allowing the accumulation of HY5 to promote photomorphogenesis Osterlund et al, 2000;Yu et al, 2013). To determine whether COP1 movement plays a role in SSG, we quantified the nuclear and cytoplasmic localization of COP1 in a transgenic line that constitutively expressed a GUS-COP1 fusion protein.…”

“…DE-ETIOLATED1 regulates the stabilization of LONG HYPOCOTYL IN FAR-RED1 (HFR1) and PHYTOCHROME INTERACTING FACTOR1 (PIF1), and the HFR1-PIF1 complex inversely modulates the entire genomic transcriptional network in phytochrome B-dependent seed germination (Shi et al, 2013(Shi et al, , 2015. CONSTITUTIVE PHOTOMOR-PHOGENESIS1 (COP1), a central repressor of light signaling, is a ring finger E3 ligase Torii et al, 1998;Jang et al, 2010;Osterlund et al, 2000;Yi and Deng, 2005), which itself is regulated by multiple factors (Zhong et al, 2009;Yu et al, 2013). Nuclear COP1 levels are attributed to dark-light transitions and are correlated with the repression of photomorphogenesis .…”

OsbZIP48, a HY5 Transcription Factor Ortholog, Exerts Pleiotropic Effects in Light-Regulated Development

“…In fact, besides Arabidopsis, the overexpression transgenics of the full-length AtHY5 orthologs in the same organism have not been raised, and that makes it difficult for us to conclude whether full-length HY5 overexpression causes semidwarfism only in rice (this study) or in other organisms too. AtHY5 is known to be involved in auxin, GA, cytokinin, ABA, ethylene, and strigolactone signaling; while it represses ethylene, GA, and auxin signaling, it promotes ABA signaling (Cluis et al, 2004;Vandenbussche et al, 2007;Alabadí et al, 2008;Chen and Xiong, 2008;Li et al, 2011b;Yu et al, 2013). In this study too, the expression of genes associated with the biosynthesis of GA, jasmonic acid, ethylene, and brassinosteroid as well as cytokinin glucosylation was altered in OsbZIP48 OE transgenics.…”

Ethylene Signaling Influences Light-Regulated Development in Pea

“…The most prominent of these are gibberellin and auxin (Casal, 2013), but ethylene has also been implicated in plant responses to light, including the regulation of hook opening, cotyledon expansion, and stem elongation (Vandenbussche et al, 2012). However, apart from detailed work on Arabidopsis hypocotyls (Yu et al, 2013), relatively few studies have examined the interaction of light and ethylene. Our characterization of an ethylene signaling mutant in pea together with the availability of several light perception and signaling mutants have provided a unique opportunity to examine this interaction in a species with hypogeal germination.…”

“…this response, ethylene is thought to promote elongation by enhancing the retention of COP1 in the light, thus increasing its activity and the degradation of its proteolytic target HY5 (Yu et al, 2013). This action of ethylene is downstream of EIN3 and therefore, EIN2, and it is possible that a similar mechanism could explain the antagonistic interaction of light and EIN2-dependent ethylene signaling on pea leaf expansion.…”