Botany online 1996-2004. No further update, only historical document of botanical science!


Ethylene

by   Margret SAUTER - Hamburg



Ethylene is a gaseous effector with a very simple structure. Nonetheless, ethylene has features that identify it as a hormone such as the fact that it is effective at nanomolar concentrations.

BLEECKER A.B. and KENDE H (2000) Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16: 1-18 (2000) http://cellbio.AnnualReviews.org/cgi/content/full/16/1/1

Biosynthesis

In higher plants, ethylene is produced from L-methionine. Methionine is activated by ATP to form S- adenosylmethionine through the catalytic actvity of S- adenosylmethionine synthetase (EC 2.5.1.6) Starting from S-adenosylmethionine two specific steps result in the formation of ethylene.The first step produces the non-protein amino acid 1-aminocyclopropane-1-carboxylic acid (ACC). It is catalyzed by ACC synthase with pyridoxal phosphate acting as a co-factor. Formation of ACC is the rate-limiting step in ethylene biosynthesis. ACC synthase (EC 4.4.1.14) is encoded by a medium-size multigene family. Various signals, which influence ethylene synthesis, result in increased expression of single members of the ACC synthase gene family. Production of ethylene from ACC is catalyzed by ACC oxidase. This reactions is oxygen-dependent. At anaerobic conditions ethylene formation is completely suppressed. Fe2+ is a co-factor and ascorbate a cosubstrate; CO2 was shown to activate ACC oxidase. ACC oxidases are encoded by small gene families in plants. (see figure to the right)

The concentration of ethylene in a plant tissue is dependent on the rate of biosynthesis and on diffusion of the gas. Ethylene is neither actively transported nor degraded. Induction of ethylene synthesis by signals such as auxin or wounding usually occurs through activation of ACC synthase through increased gene expression. ACC oxidase activity on the other hand is constitutively present in most vegetative plant tissues. In some cases, further induction of ACC oxidase by ethylene is observed.

Auxin has been shown to stimulate ethylene formation in various plant tissues. In etiolated pea seedlings (Pisum sativum L.), these two hormones are involved in the formation of the apical hook of the hypocotyl. An asymmetric distribution of auxin is thought to result in elevated ethylene synthesis at the site of higher auxin concentration. High levels of ethylene in turn inhibit growth on that side resulting in curvature of the hypocotyl.

In maturing fruits, ethylene synthesis is autocatalytically enhanced, i.e., ethylene induces its own biosynthesis. The self-enhancing synthesis and diffusion of the gaseous hormone throughout the fruit accelerate ripening and contribute to a synchronized ripening process.

Distribution

Probably each plant tissue produces or takes up ethylene at some point during development and responds to it in an appropriate fashion. Uptake is usually not a problem because ethylene can diffuse freely through membranes. Distribution of the gas within the plant occurs through intercellular spaces and when dissolved in the symplast from cell to cell. Long-distance distribution is achieved by releasing ACC into the vascular tissue where it is moved to the site of action. There, is converted to ethylene. Tomatoes, for instance, produce ACC in water-logged roots. ACC is moved via the vascular bundles to the leaves where it is converted to ethylene, which then induces epinastic lowering of the petioles.

Ethylene - perception and signaling

Ethylene action very often involves transcriptional activation. In recent years, much has been learned about the transduction pathway from ethylene perception to gene activation. Ethylene is bound by a receptor that is membrane-localized. The N-terminal domain of the receptor protein is responsible for binding of ethylene. The intracellular portion of the protein is a protein kinase which is activated upon binding of ethylene. Such receptor protein kinases are termed two-component-systems because they are generally composed of a sensor, in this case the ethylene binding site, and a response regulator. Two-component-receptors have first been characterized in bacteria, but are now also known from plants. The first two-component-receptor to be discovered in plants was the ethylene receptor ETR1 (ethylene resistant 1) from Arabidopsis thaliana L.. Transduction of the ethylene signal is thought to be achieved through a series of phosphorylations that are carried out by a cascade of protein kinases similar to the MAP (mitogen activated protein kinase) kinase pathway and probably through other, as yet less well defined, steps. Finally, a transcription factor that is present in the cell is activated leading to induction of one or more early gene(s). One such early gene is itself a transcriptional activator that induces late genes. These late-induced genes may encode enzymes which degrade the middle lamellae or the cell wall during fruit ripening and abscission They may encode for proteins involved in pathogen defense. Or they may encode for proteins required for other ethylene responses.

Ethylene acts as a negative regulator of the signaling pathway. This means, that the signal pathway is turned on in the absence of ethylene and is shut down when ethylene is present. Shutting down of the pathway induces an ethylene response. As a result of this negative regulation, mutations in the ethylene receptor are perceived as dominant gain-of-function mutations.

Inhibitors

Inhibitors are frequently used to study biosynthesis of ethylene and ethylene activity. AVG (aminoethoxyvinylglycine) und AOA (aminooxy-acetic acid) are inhibitors of ethylene biosynthesis. NBD (2, 5-norbornadiene) and Ag+ inhibit an ethylene response by binding to and blocking of the ethylene receptor. NBD is more specific as compared to silver ions.

Responses

Ethylene promotes maturation and abscission of fruits. This has been known since early last century. Since 1934, it is known that plants themselves can produce ethylene. Many climacteric fruits such as apple, banana and tomato show a strong increase in ethylene levels at the late green or breaker stage. As a consequence of high ethylene chlorophyll is degraded and other pigments are being produced. This results in the typical color of the mature fruit peel. Activity of many maturation-related enzymes increases. Starch, organic acids and in some cases, such as avocado lipids, are mobilized and converted to sugars. Pectins, the main component of the middle lamella are degraded. The fruit softens. These metabolic activities are accompanied by a high respiration rate and consequently by high oxygen consumption. Ethylene levels are especially high in the separating tissues resulting in abscission of the fruit.

In addition, ethylene regulates senescence and fading of flowers and abscission of petals and leaves. In most cases, flower formation is inhibited by ethylene. Pineapple (Bromeliaceae) is exceptional in that ethylene promotes flower formation.

Ethylene has evolved as the central regulator of cell death programs in plants. In roots and in some plants in stems, lack of oxygen induces formation of intercellular spaces, the so-called aerenchyma. Low oxygen conditions in waterlogged roots, for instance, result in lysogenous aerenchyma formation through programmed death of cells in the cortex. This process is controlled by ethylene, as is programmed death of endosperm cells during cereal seed development.

Biotic and abiotic stresses frequently result in formation of ethylene. The physiological responses to stress ethylene can be rather divers. In some cases disease symptoms are boosted; in some cases they are ameliorated. And yet in other cases stress ethylene does not result in obvious responses.

Ethylene regulates not only senescence-related processes in plants but also growth responses such as asymmetric growth of the hypocotyl hook in dicotyledonous plants or agravitropic growth of the stem. As a general rule, ethylene acts as a growth inhibitor in terrestric plants.

In semiaquatic plants, however, ethylene promotes growth. H. KENDE (Michigan State University,USA; MÉTRAUX and KENDE, 1983, KENDE et al., 1998) chose rice (Oryza sativa L.) as an experimental system to study the growth response of this semiaquatic crop plant. Most rice varieties are grown in flooded fields. Deepwater rice varieties are grown in areas where water levels rise even more during the rainy season. In these plants, partial submergence induces rapid growth of the stem. In this way, deepwater rice plants manage to keep part of their leaves above the rising water level and to supply the submerged plant parts with oxygen. Growth induction is mediated by ethylene. Ethylene has a very low diffusion rate in water and accumulates in submerged plant parts. In addition to limited diffusion from the plant, ethylene synthesis is induced by submergence. Both, ACC synthase and ACC oxidase activities increase as a result of low oxygen tension. Ethylene, in turn, increases gibberellin synthesis and sensitivity of the tissue towards gibberellin. Physiologically effective concentrations of gibberellin are ultimately responsible for growth induction in the internode of the rice stem. Growth rates of up to 25 cm per day are achieved through an approximately threefold higher rate of cell division and through increased cell elongation including threefold longer cells. Ethylene thus acts as an intermediary signal between hypoxia and gibberellin in the transduction pathway that leads from submergence to internodal growth.

Applications

When fruits are stored in closed rooms, ethylene that is released from ripening and mature fruits accumulates and stimulates late-ripening fruits to premature ripening ("One rotten apple can ruin the whole basket"). For fruit storage, it is favorable to avoid formation or spread of ethylene. Therefore, fruits are often stored under hypobaric conditions to remove ethylene that is released. Conversely, banana are harvested, transported, and stored at an immature stage. Before being shipped to stores, they are treated with ethylene to induce synchronous ripening.

Biotechenological strategies have also been persued to control ethylene action on fruit ripening and on fading of petals. One approach taken in tomato was designed to inhibit biosynthesis of ethylene within the plant. This was achieved by antisense expression of ACC synthase or ACC oxidase. Depletion of the ACC pool through ectopic expression of a bacterial ACC deaminase gene was also successful in reducing ethylene formation. In a second approach, a mutated ethylene receptor from Arabidopsis was introduced into tomato and petunia. This resulted in delayed fruit ripening, delayed petal fading, and in delayed flower abscission.


© Peter v. Sengbusch - Impressum