Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seedlings

Abstract

Dark-grown Arabidopsis seedlings develop an apical hook when germinating in soil, which protects the cotyledons and apical meristematic tissues when protruding through the soil. Several hormones are reported to distinctly modulate this process. Previous studies have shown that ethylene and gibberellins (GAs) coordinately regulate the hook development, although the underlying molecular mechanism is largely unknown. Here we showed that GA 3 enhanced while paclobutrazol repressed ethylene-and EIN3-overexpression (EIN3ox)-induced hook curvature, and della mutant exhibited exaggerated hook curvature, which required an intact ethylene signaling pathway. Genetic study revealed that GA-enhanced hook development was dependent on HOOKLESS 1 (HLS1), a central regulator mediating the input of the multiple signaling pathways during apical hook development. We further found that GA 3 induced (and DELLA proteins repressed) HLS1 expression in an ETHYLENE INSENSITIVE 3/EIN3-LIKE 1 (EIN3/ EIL1)-dependent manner, whereby EIN3/EIL1 activated HLS1 transcription by directly binding to its promoter. Additionally, DELLA proteins were found to interact with the DNA-binding domains of EIN3/EIL1 and repress EIN3/EIL1-regulated HLS1 expression. Treatment with naphthylphthalamic acid, a polar auxin transport inhibitor, repressed the constitutively exaggerated hook curvature of EIN3ox line and della mutant, supporting that auxin functions downstream of the ethylene and GA pathways in hook development. Taken together, our results identify EIN3/EIL1 as a new class of DELLA-associated transcription factors and demonstrate that GA promotes apical hook formation in cooperation with ethylene partly by inducing the expression of HLS1 via derepression of EIN3/EIL1 functions.

Large-Scale Identification of Gibberellin-Related Transcription Factors Defines Group VII ETHYLENE RESPONSE FACTORS as Functional DELLA Partners

“…A combined treatment of wild-type etiolated seedlings with 12.5 mM ACC plus 1 mM GA 4 provoked the formation of hooks with an exaggerated curvature ( Fig. 6B; Gallego-Bartolomé et al, 2011;An et al, 2012). Remarkably, rap2.3 mutant seedlings were partially resistant to treatment with both hormones, and the hook angle was significantly reduced in the mutant compared with the wild type, having a similar angle to that observed when ACC alone is supplied (Fig.…”

Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling inArabidopsis

“…HOOKLESS1 (HLS1) is a central positive regulator of apical hook development (Lehman et al, 1996;An et al, 2012) (Figures 1A and 1B). The mutants eto1-1 and ctr1-1, with high level of HLS1 expression, exhibited exaggerated hook curvature, while the mutant ein3-1 eil1-3, with low levels of HLS1 expression, displayed reduced hook curvature (Figures 1A and 1B).…”

“…Both ethylene (ET) and jasmonate (JA) are essential plant hormones that regulate various plant developmental processes and diverse defense responses (Kieber, 1997;Bleecker and Kende, 2000;Guo and Ecker, 2004;Broekaert et al, 2006;Howe and Jander, 2008;Browse, 2009;Shan et al, 2012;Wasternack and Hause, 2013). ET signal is perceived by its receptors ETHYLENE RESPONSE1 (ETR1), ETR2, ETHYLENE RESPONSE SENSOR1 (ERS1), ERS2, and ETHYLENE INSENSITIVE4 (EIN4) (Hua and Meyerowitz, 1998) to repress CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) (Kieber et al, 1993), which activates EIN2 (Alonso et al, 1999;Ju et al, 2012;Qiao et al, 2012;Wen et al, 2012) and subsequently stabilizes EIN3 and EIN3-LIKE1 (EIL1) (Chao et al, 1997;Guo and Ecker, 2003;Potuschak et al, 2003;Gagne et al, 2004) to mediate various ET responses, including hypocotyl growth (Zhong et al, 2012), apical hook formation (Knight et al, 1910;An et al, 2012), root growth (Ortega-Martínez et al, 2007;Růzicka et al, 2007), flowering (Ogawara et al, 2003;Achard et al, 2007), fruit ripening (Burg and Burg, 1962;Theologis et al, 1992), leaf senescence (Gepstein and Thimann, 1981;Li et al, 2013), freezing tolerance , and resistance against pathogen infection (Alonso et al, 2003;Chen et al, 2009).…”

ETHYLENE-INSENSITIVE3 Is a Senescence-Associated Gene That Accelerates Age-Dependent Leaf Senescence by Directly Repressing miR164 Transcription in Arabidopsis

“…We performed chromatin immunoprecipitation (ChIP) experiments using iE/qm plants to test this possibility. We chose three regions in the miR164A promoter containing putative EBSs (TACAT or TTCAAA) (Itzhaki et al, 1994;Konishi and Yanagisawa, 2008;Zhong et al, 2009;An et al, 2012) (Figure 6A). We found marked enrichment of EIN3 in these EBS regions, particularly the P2 site (TACAT), indicating that EIN3 binds to this region in vivo ( Figure 6B).…”