Ethylene, a key factor in the regulation of seed dormancy

Abstract

Ethylene is an important component of the gaseous environment, and regulates numerous plant developmental processes including seed germination and seedling establishment. Dormancy, the inability to germinate in apparently favorable conditions, has been demonstrated to be regulated by the hormonal balance between abscisic acid (ABA) and gibberellins (GAs). Ethylene plays a key role in dormancy release in numerous species, the effective concentrations allowing the germination of dormant seeds ranging between 0.1 and 200 μL L(-1). Studies using inhibitors of ethylene biosynthesis or of ethylene action and analysis of mutant lines altered in genes involved in the ethylene signaling pathway (etr1, ein2, ain1, etr1, and erf1) demonstrate the involvement of ethylene in the regulation of germination and dormancy. Ethylene counteracts ABA effects through a regulation of ABA metabolism and signaling pathways. Moreover, ethylene insensitive mutants in Arabidopsis are more sensitive to ABA and the seeds are more dormant. Numerous data also show an interaction between ABA, GAs and ethylene metabolism and signaling pathways. It has been increasingly demonstrated that reactive oxygen species (ROS) may play a significant role in the regulation of seed germination interacting with hormonal signaling pathways. In the present review the responsiveness of seeds to ethylene will be described, and the key role of ethylene in the regulation of seed dormancy via a crosstalk between hormones and other signals will be discussed.

Keywords: abscisic acid; dormancy; ethylene; gibberellins; reactive oxygen species; seed germination.

FIGURE 1

Ethylene biosynthesis and signaling pathways. S-adenosyl methionine (S-AdoMet) is synthesized from methionine by the SAM synthetase, it is then converted to 1-aminocyclopropane-1-carboxylic acid (ACC) by the ACC synthase (ACS), 5-methylthioadenosine (MTA) being a by-product. MTA is recycled to methionine through the Yang Cycle by successive enzymatic reactions involving different intermediates among which 5-methylthioribose (MTR) and 2-keto-4-methylthiobutyrate (KMB). S-AdoMet is also the precursor of the spermidine/spermine biosynthesis pathway. Ethylene production results from the ACC oxidation catalyzed by the ACC oxidase (ACO) that also generates carbon dioxide and cyanide. Malonylation of ACC to malonyl-ACC (MACC) reduces ACC content and consequently ethylene production. Ethylene can stimulate its own biosynthesis, by improving ACC synthesis catalyzed by ACS, and conversion to ethylene by ACO. Ethylene binds to receptors (among which ethylene receptor 1, ETR1) located in the endoplasmic reticulum, which leads to the deactivation of the receptors that become able to recruit CTR1 (constitutive triple response). Release of CTR1 inhibition allows EIN2 to act as a positive regulator of ethylene signaling pathway. EIN2 acts upstream of nuclear transcription factors, such as EIN3 (ethylene insensitive), EILs (EIN3-like), ERBPs (ethylene responsive element binding protein), and ERFs (ethylene response factor). → and —∙ arrows indicate positive and negative interactions between the different elements of the signaling cascade, respectively.

FIGURE 2

Interactions between ethylene, abscisic acid, gibberellins, and ROS in the regulation of seed germination and dormancy. This scheme is based on genetic analyses, microarray data, and physiological studies on seed responsiveness to ethylene, ABA, GAs, or ROS cited in the text. Ethylene down-regulates ABA accumulation by both inhibiting its synthesis and promoting its inactivation or catabolism, and also negatively regulates ABA signaling. ABA inhibits ethylene biosynthesis through ACS and ACO activities. Ethylene also improves the GAs metabolism, and GAs signaling, and vice versa. ROS enhance ABA catabolism and both C₂H₄ and GAs signaling. Whether ROS are signals induced by environmental factors to modulate the hormonal network toward germination is to be investigated. → and —∙ arrows indicate positive and negative interactions between the different elements of the signaling cascade, respectively.