(1979) pp KILLEY D.R. Ethylene and Ethylene Physiolgy.
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1 (1979) pp KILLEY D.R. Ethylene and Ethylene Physiolgy.
2
3 Reprint from Plant Growth Substances 1979 Edited by F. Skoog Springer-Verlag Berlin Heidelberg 1980 Printed in Germany. Not for Sale. Springer-Verlag Berlin Heidelberg New York
4 Ethylene and Ethylene Physiology D.R. DILLEY 1 Ethylene, indeed, is a busy gas. So busy, in fact, that seemingly, each month when the professional journals are published, some new involvement is discovered or a new application for ethylene in agriculture is developed. Prior to the 1950's, about the only commercial use of ethylene in agriculture was gassing mature green bananas and tomatoes to make them ripen. Limited application was made of the use of ethylene-saturated water to induce flowering in pineapple. Today there is an ever-growing long list of uses and potential uses for ethylene (10, 14), making it one of the most widely used plant growth regulators in agriculture. This has come about through a better understanding of ethylene's role in plant physiology (6, 12) and through the development and use of agricultural chemicals such as ethephon, which when applied to crop plants evolve ethylene gas. Ethrel and CEPA are commercial formulations of ethephon in widespread use today. The widespread interest in ethylene as a plant growth regulator stems from the fact that so many physiological processes are either stimulated or inhibited in the presence of the gas (1,14). Moreover, the direction of the ethylene effect can sometimes change depending upon concentration and/or stage of plant development at the time the application is made. While there is a wide variety of plant responses favorably affected by ethylene_, there are numerous examples where the effects may be adverse or premature in terms of crop utilization. This has led to interest in developing means to attenuate ethylene biosynthesis, inhibit ethylene action, or remove ethylene from the atmosphere (1). Ethylene is a natural component of the atmosphere; clean ambient air contains 5-20 ppb, crop canopy levels of 80 ppb are recorded, and levels in excess of 300 ppb are commonly found in urban and industrial areas as a pollutant from fossil fuel combustion (1). These ambient ethylene levels become important when one considers that some plant responses are seen at ethylene levels as low as 20 ppb and most plant responses are half-maximally affected at a concentration of 100 ppb. The concentration of ethylene as a dissolved gas in water at room temperature in equilibrium with 100 ppb ethylene in the atmosphere is approximately 1 x M. This is several orders of magnitude lower than the concentration at which most other plant growth regulators are active. In many, but not all, of the processes ethylene has been found to stimulate or attenuate, it does so as an endogenous plant hormone. These range from stimulating seed germination to causing fruit ripening and senescence. The manifold effects include: 1 Horticulture Depru:trnent, Michigan State University, East Lansing, Michigan 48824, USA
5 Ethylene and Ethylene Physiology Breaking of seed and bud dormancy Root initiation Hypocotyl hook formation and strengthening Stem strengthening Internode shortening Lateral branching Leaf epinasty 393 Flower initiation Modif1cation of flower sex Flower and fruitlet thinning Fruit growth stimulation Fruit ripening, abscission, and senescence Fruit and leaf degreening Leaf abscission and senescence Ethylene effects thus span all phases of plant development. Examples of important applications of ethylene in agriculture involving effects in different developmental phases will be discussed briefly. Seed Germination and Breaking of Dormancy Dormancy of certain seeds requiring light for germination can be broken by ethylene treatment. Ethylene also helps overcome high-temperature inhibition of germination of some seeds. Apart from breaking of dormancy, an absolute requirement for ethylene in germination has not been demonstrated. Bud dormancy of certain fruit trees requiring chilling is broken by ethylene. This is sometimes seen prematurely following heat or drought stress which induces ethylene synthesis, and causes some trees and shrubs to bloom in the fall rather than remain dormant until spring. Dormancy of buds on rhizomes of weeds such as quackgrass, Johnsongrass, and nutgrass is broken by ethylene, and this has some practical value in stimulating early growth for more effective herbicide application (15). Rooting of cuttings of some plants can be improved if the plants or cuttings are first treated with ethylene. Ethylene does not seem to playa direct role in these responses but rather may exert its effects by altering the distribution of auxin. Seedling Development Ethylene may inhibit or stimulate stem growth (17). It causes hypocotyl hook formation and maintenance. Mechanical impedance of the growth of the seedling by a soil crust causes an increase in ethylene production. This slows elongation and promotes radial growth which strengthens the stem and allows the seedling to break through the soil crust. Stem elongation of certain aquatic plants is stimulated by ethylene. Ethylene accumulates in the hollow stem of these submerged plants and the stem continues to elongate until the frond reaches the surface, at which time the gas is released and stem elongation ceases. Ethylene acts as a modulator of growth in these instances. Vegetative Growth There are numerous examples of ethylene effects in the vegetative growth phase (17). These include: growth inhibition, leaf epinasty, induction of rooting, release of apical
6 394 D.R. Dilley dominance, promotion of tillering and rhlzome growth, stem stiffening, and latex flow. Some effects are important agronomically or horticulturally. Inhibition of terminal growth improves the appearance and value of plants such as azalea and poinsettia by increasing lateral branching and making a more compact flowering plant. Lodging in small grains can be attenuated by ethylene. This is an important commercial use of ethephon. Release from apical dominance by ethylene allows lateral and basal buds of Kentucky bluegrass turf plants to grow, helping to improve the stand. Latex flow in rubber trees is stimulated by applying ethephon to the bark below the tapping cut (4). This markedly increases rubber yields by increasing latex flow, saving labor by reducing the tapping frequency, and by prolonging the life of the rubber tree by allowing shorter tapping cuts. This application has become the most important commercial use of Ethrel. Flowering and Fruiting Flowering of certain plants is promoted by ethylene. This is true of pineapple (18) and some ornamental bromeliads. In the case of pineapple, treatment of fields with ethephon induces uniform flower formation which is essential for scheduling harvest (10). Flower bud formation is indirectly stimulated in young fruit trees by suppressing vegetative growth with an ethephon application made early in the growing season. This helps to bring orchards into bearing as much as a year or two earlier then normal. By promoting abscission of flowers and fruits, ethylene can be used as a thinning agent for fruits and to remove nuisance fruits in lawns and gardens (10). Female sex expression in cucurbits is promoted by ethylene. In fact, ethylene appears to playa definitive role in this respect (9). Promotion of female flowers and elimination of male flowers by ethephon is important in hybridizing to prevent selfpollination of some crops. In commercial cucurbit production the increased femaleness can also result in earlier and increased yields (10,14). Postharvest aspects of ethylene physiology are particularly important and have been widely investigated. While most of what has gone before dealt with effects of ethylene that contribute in a positive way to plant growth and development and accrue positively with respect to productivity or quality, most of the postharvest aspects of ethylene affect the commodity in a negative sense from the handler's standpoint. This is a natural consequence of ethylene's role in promoting senescence of plants and plant organs: a role that may have survival value to the species but may interfere in postharvest commodity preservation. A number of approaches are potentially useful and some are commercially employed to attenuate the effect of ethylene after harvest. The role of ethylene in accelerating senescence of fruits, vegetables, and flowers has been recognized for many years (1, 12). Many of the storage and handling procedures that have been developed for these commodities directly or indirectly subdue the synthesis or action of ethylene in its natural role as a ripening or senescence promoting agent (11). These include the use of controlled atmosphere storage at refrigerated temperatures, which diminishes the rate of ethylene production by lowering the O 2 level to below 3%, and inhibits the action of ethylene by elevating the CO 2 in the storage atmosphere to 3%-5%. This technique is used to prolong the storage life and
7 Ethylene and Ethylene Physiology 395 delay ripening of over 30 million bushels of apples annually in the USA and Canada alone. Inhibition of ethylene action by CO 2 is widely recognized in cut flowers such as carnations. Recognition of the central role of ethylene has led to past attempts to reduce the concentration of ethylene surrounding stored commodities by ventilation, absorption, or destruction. However, the concentration of ethylene within the tissue is governed by its production rate and the diffusion rate from the tissue. Although the external ethylene concentration can be reduced to negligible levels, sufficient gas remains in most tissues to cause a response, since only as little as 50 ppb of ethylene is required to cause a half-maximal effect in some tissues (6). Hypobaric or Low Pressure Storage Studies of the gas exchange process in fruits by Burg and Burg (7) led to the observation that ethylene or CO 2 produced within the organ escapes through an aircfllied pore or opening, such as a stoma or lenticel, more readily when the commodity is subjected to a low-molecular-weight gaseous atmosphere. Although the rate of gas production was not affected, gas diffusion was facilitated because the density of the media through which diffusion occurred was lowered. Gas diffusion coefficients are inversely proportional to the molecular weight of the diffusion media and to atmospheric pressure. Thus, by lowering the atmospheric pressure to 0.1 atmosphere, ethylene, CO 2, and other volatiles escape from the tissue 10 times more rapidly than into air at atmospheric pressure. This, together with the lowered O 2 supply, reduces the equilibrium concentration of ethylene and some other gasses produced within tissues by at least a factor of 10. These studies led to the development of hypobaric storage (8). This subject was recently reviewed (13). In actual practice, and on a limited commercial scale, the commodity is placed in a vacuum-tight, refrigerated container and evacuated by a vacuum pump to the desired low pressure which, depending upon the commodity, may vary from 10 mm Hg to 76 mm Hg. The oxygen level varies in direct response to the absolute pressure. When the desired low pressure is obtained, fresh air is admitted to the chamber through a pressure regulator and then humidified. In the continuously ventilated partial vacuum, carbon dioxide, ethylene, and waste volatile by -products of metabolism rapidly diffuse out of the commodity and are flushed from the storage chamber. Hypobaric storage technology is being developed commercially by Grumman Allied Industries. Inc. There are several consequences of ventilating a commodity at hypobaric pressure: (i) Oxygen supply is reduced and this reduces the respiration rate and ethylene synthesis. (ii) Ethylene, which the tissues produce and which causes them to ripen or senesce, is removed from the tissue and flushed out of the storage. Hence, deterioration is delayed. (iii) Other volatile substances produced by the fruit such as carbon dioxide, acetaldehyde, acetic acid, esters, and a-farnesene (a terpene) are swept from the fruit. Acetic acid and acetaldehyde have been implicated in the development of internal breakdown and a-farnesene has been related to superficial scald of some fruits.
8 396 D.R. Dilley: Ethylene and Ethylene Physiology Inhibitors of Ethylene Synthesis and Action Another approach to attenuate ethylene effects is to reduce or inhibit the synthesis of ethylene in the tissue specifically or to block the action of the gas. Aminoethoxyvinylglycine (A VG), an analog of the antibiotic rhizobitoxine, is a rather specific inhibitor of ethylene biosynthesis from methionine (12). It blocks the conversion of s-adenosylmethionine to 1-aminocyclopropane-l-carboxylic acid (ACC), which is the immediate precursor of ethylene in plants (2). Processes such as fruit ripening and flower senescence are retarded by treatment with A VG, but commercial use of A VG should be approached with caution because of the broad range of other reactions that may be affected. Ag+ has been found to be a very potent inhibitor of ethylene action (3). It is effective at low concentrations when applied as a dip or foliar spray to the tissue, and it prevents ethylene action in a broad range of responses including fruit ripening and flower fading. Cost as well as potential toxicity to man will limit practical uses of Ag+. A substituted benzothiadiazole also inhibits ethylene action in a number of responses (19). It apparently inhibits ethylene action (9), although ethylene synthesis can be stimulated by the compound. In summary, ethylene is the gaseous plant hormone that is active in physiological and morphological processes at virtually all stages of plant development from seed germination through senescence. Environmental, mechanical, and chemical factors may attenuate or stimulate ethylene synthesis or action. Numerous important agronomic and horticultural practices have evolved and continue to be developed with increasing recognition of the role of ethylene in plant growth and development. References L Abeles, F.B.: Ethylene in Plant Biology. London, New York: Academic Press Adams, D.O., Yang, S.F.: Proc. Natl. Acad. Sci. USA 76, (1979) 3. Beyer, E.M.: Plant Physiol. 58, (1976) 4. Blencoe, l.w.: World Crops 23, f (1971) 5. Bukovac, M.J.: HortScience 6, (1971) 6. Burg, S.P.: Proc. NatL Acad. Sci. USA 70, (1973) 7. Burg, S.P., Burg, E.A.: Physiol. Plant. 18, (1965) 8. Burg, S.P., Burg, E.A.: Science 153, (1966) 9. Byers, R.E., Baker, L.R., Sell, H.M., Herner, R.C., Dilley, D.R.: Proc. Natl. Acad. Sci USA 69, (1972) 10. de Wilde, R.C.: HortScience 6, (1971) 11. Dilley, D.R.: J. Food Biochem. 2, (1979) 12. Lieberman, M.: Annu. Rev. Plant Physiol. 20, (1979) 13. Lougheed, E.C., Muir, D.P., Berard, Luce: HortScience 13,21-27 (1978) 14. Morgan, P.W.: Acta Hortic. 34,41-54 (1973) 15. Morgan, P.W.: In: Herbicides: Physiology, Biochemistry, Ecology. Audus, L.J. (ed), vol. I, pp London, New York: Academic Press 1976,608 pp. 16. Poovaiah, B.W., Leopold, A.C.: Crop Sci. 13, (1973) 17. Pratt, H.K., Goeschl, J.D.: Annu. Rev. Plant Physiol. 20, (1969) 18. Traub, H.P., Cooper, W.c., Reece, P.C.: J. Am. Soc. Hortic. Sci. 37, (1939) 19. Van Daalen, J.J., Daams, J.: Naturwissenschaften 8, 395 (1970)
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