Modulation of Organogenesis and Somatic Embryogenesis by Ethylene: An Overview

Abstract

Ethylene is a plant hormone controlling physiological and developmental processes such as fruit maturation, hairy root formation, and leaf abscission. Its effect on regeneration systems, such as organogenesis and somatic embryogenesis (SE), has been studied, and progress in molecular biology techniques have contributed to unveiling the mechanisms behind its effects. The influence of ethylene on regeneration should not be overlooked. This compound affects regeneration differently, depending on the species, genotype, and explant. In some species, ethylene seems to revert recalcitrance in genotypes with low regeneration capacity. However, its effect is not additive, since in genotypes with high regeneration capacity this ability decreases in the presence of ethylene precursors, suggesting that regeneration is modulated by ethylene. Several lines of evidence have shown that the role of ethylene in regeneration is markedly connected to biotic and abiotic stresses as well as to hormonal-crosstalk, in particular with key regeneration hormones and growth regulators of the auxin and cytokinin families. Transcriptional factors of the ethylene response factor (ERF) family are regulated by ethylene and strongly connected to SE induction. Thus, an evident connection between ethylene, stress responses, and regeneration capacity is markedly established. In this review the effect of ethylene and the way it interacts with other players during organogenesis and somatic embryogenesis is discussed. Further studies on the regulation of ERF gene expression induced by ethylene during regeneration can contribute to new insights on the exact role of ethylene in these processes. A possible role in epigenetic modifications should be considered, since some ethylene signaling components are directly related to histone acetylation.

Keywords: S-adenosylmethionine; ethylene biosynthesis; ethylene inhibitors; in vitro culture; plant hormones; stress responses.

Figure 1

Schematic overview of ethylene biosynthesis and the canonical signaling pathway. Ethylene acts as an inverse agonist, inhibiting its receptors. This inhibition leads to a reduction in CTR1 activity, which allows the set of reactions downstream to occur, culminating in ethylene responses. The different pathways are separated by a dashed line. Inhibition steps are marked with an inhibitory arrow (red). Based on the signaling models of Wang et al. [10] and Binder [15].

Figure 2

Schematic diagram of some of the principal ethylene modulators and their points of action. Ethylene precursors are shown in green followed by a green arrow. Inhibitors of ethylene biosynthesis and action are shown in orange followed by an inhibitory arrow (red). Dashed arrows indicate the pathway steps that can be affected by modulation. Based on Schaller and Binder [22].

Figure 3

Possible molecular framework for the effect of ethylene on SE process. Exogenous auxins enhance ethylene production in response to stress. Specific transcriptional factors from the ERF family are activated, leading to an increase in LEC and YUC expression levels and consequent SE induction—based on the molecular mechanisms proposed by Nowak et al. [130] in Arabidopsis and the studies of Ikeuchi et al. [3]. In an auxin-free medium, ethylene production decreases, leading to an increase in YUC levels and somatic embryo development—based on Arabidopsis studies [129]. In the presence of auxin, somatic embryo development depends on the specific ERFs to be induced, SERF1 and GL15, perhaps as a consequence of stress induced by auxins and cytokinins—based on studies in Mendicago truncatula [131] and soybean [113].