The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes

Abstract

The length of the Arabidopsis thaliana life cycle depends on the timing of the floral transition. Here, we define the relationship between the plant stress hormone ethylene and the timing of floral initiation. Ethylene signaling is activated by diverse environmental stresses, but it was not previously clear how ethylene regulates flowering. First, we show that ethylene delays flowering in Arabidopsis, and that this delay is partly rescued by loss-of-function mutations in genes encoding the DELLAs, a family of nuclear gibberellin (GA)-regulated growth-repressing proteins. This finding suggests that ethylene may act in part by modulating DELLA activity. We also show that activated ethylene signaling reduces bioactive GA levels, thus enhancing the accumulation of DELLAs. Next, we show that ethylene acts on DELLAs via the CTR1-dependent ethylene response pathway, most likely downstream of the transcriptional regulator EIN3. Ethylene-enhanced DELLA accumulation in turn delays flowering via repression of the floral meristem-identity genes LEAFY (LFY) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1). Our findings establish a link between the CTR1/EIN3-dependent ethylene and GA-DELLA signaling pathways that enables adaptively significant regulation of plant life cycle progression in response to environmental adversity.floral transition ͉ Arabidopsis thaliana ͉ LFY ͉ gibberellin F loral initiation is a major step in the plant life cycle (1). Accordingly, plants have evolved mechanisms for regulating the timing of floral initiation. These mechanisms permit an adaptively significant integrated response to multiple interacting factors (both internal and external to the plant). In essence, the endogenous developmental competence of plants to flower is integrated with environmental cues that signal the onset of conditions favorable for reproductive success (2).In this article, we describe the role of the gaseous phytohormone ethylene in the regulation of floral initiation. Ethylene is already known to modulate Arabidopsis vegetative environmental growth responses (3-5). For example, adverse environmental conditions enhance ethylene production, and thereby restrain growth (3, 4). Ethylene is perceived by the ETR1 family of ethylene receptors (6-10). In the absence of ethylene, ETR1 activates CTR1, a Ser/Thr kinase (closely related to the RAF kinases) that is a negative regulator of ethylene signaling (11,12). Downstream of CTR1 are several positive regulators of ethylene response: EIN2 (a membrane-associated protein whose function is not clear; ref. 13) and the EIN3 and EIN3-like (EIL) transcription factors (14, 15). EIN3 regulates ethylene-responsive genes (6, 15), whereas overexpression of EIN3 results in the constitutive activation of ethylene responses (14). Furthermore, ethylene response depends on EIN3 stability. In the absence of ethylene, EIN3 degradation is promoted by a specific Skp1-cullin-F box protein (SCF) E3 ubiquitin ligase (SCF EBF1/EBF2 ) that targets EIN3 for destruction by the proteasome (16-18). Howev...

Global Identification of DELLA Target Genes during Arabidopsis Flower Development

“…Since RGA upregulated genes include those encoding the regulators in the ethylene signaling pathway, such as ERS2 and SR1, ethylene control of anther dehiscence would be more or less modulated by RGA. On the other hand, ethylene inhibits root growth and flowering in Arabidopsis partly by enhancing the accumulation of DELLA proteins (Achard et al, 2003(Achard et al, , 2006(Achard et al, , 2007. Thus, anther dehiscence could also be mediated through the effect of ethylene on the stabilization of DELLA proteins.…”

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

“…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).…”

EIN2 mediates direct regulation of histone acetylation in the ethylene response

“…It is important in responses to stress, such as drought, cold, flooding, and pathogen infection (1,2), and modulates stem cell division (3). The common aquatic ancestor of plants possessed the ethylene signaling pathway and the mechanism has been elucidated by analysis of Arabidopsis (4).…”