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Ethylene in Plant Growth

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Ethylene in Plant Growth Proc. Nat. Acad. Sci. USA Vol. 70, No. 2, pp. 591-597, February 1973 Ethylene in Plant Growth STANLEY P. BURG The Fairchild Tropical Garden, and University of Miami, Miami, Florida 33156 ABSTRACT Ethylene inhibits cell division, DNA syn- of ethylene in plant growth destined to be studied intensively thesis, and growth in the meristems of roots, shoots, and axillary buds, without influencing RNA synthesis. Apical again. dominance often is broken when ethylene is removed, ap- Effects of ethylene on cell division parently because the gas inhibits polar auxin transport ir- reversibly, thereby reducing the shoot's auxin content just When etiolated pea seedlings are grown continuously in the as if the apex had been removed. A similar mechanism presence of a trace of ethylene, the stem hardly elongates and may underly ethylene-induced release from dormancy of root growth is inhibited about 60% (refs. 2, 5, 6; Fig. 3). A buds, tubers, root initials, and seeds. Often ethylene in- hibits cell expansion within 15 min, but delays differentia- swollen zone develops behind the root tip, root hairs prolifer- tion so that previously expanding cells eventually grow to ate, and the root deflects plageotropically in the gravitational enormous size. These cells grow isodiametrically rather field (5-7); similar changes occur in the stem (2, 5, 6). The than longitudinally because their newly deposited cellu- major cause of the overall growth inhibition is cessation or lose microfibrils are laid down longitudinally rather than retardation of the mitotic process in the meristems of the radially. Tropistic responses are inhibited when ethylene root, reversibly and rapidly prevents lateral auxin transport. In shoot, and axillary buds (5, 6). Within a few hours after most of these cases, as well as certain other instances, ethylene is applied, the number of mitotic figures in the stem ethylene action is mimicked by application of an auxin, apex begins to decline, and within about 10 hr mitosis almost since auxins induce ethylene formation. Regulation by stops. Auxins such as 2,4-dichlorophenoxyacetic acid (2,4-D) ethylene extends to abscission, to flower formation and cause fading, and to fruit growth and ripening. Production of the same effect, at least in part by stimulating ethylene ethylene is controlled by auxin and by red light, auxin production in the apex. Ethylene inhibits mitosis in the root acting to induce a labile enzyme needed for ethylene syn- apex by about 60% and 2,4-D has a similar effect, but very thesis and red light to repress ethylene production. Nu- high concentrations of 2,4-D stimulate mitosis in the elon- merous cases in which a response to red light requires an gating zone of the root just as in the elongating zone of the intervening step dependent upon inhibition of ethylene production have been identified. Ethylene action requires stem. These divisions give rise to root initials in both tissues, noncovalent binding of the gas to a metal-containing and ethylene does not interfere with their formation, although receptor having limited access, and produces no lasting it slows their outgrowth. Both auxin (8) and ethylene (5) product. The action is competitively inhibited by C02, and block cell division in meristems at some stage before prophase, requires 02. Ethylene is biosynthesized from carbons 3 and 4 of methionine, apparently by a copper-containing en- and auxins appear to function in this case through an inter- zyme in a reaction dependent upon an oxygen-requiring vening step in which ethylene is produced. Within a few hours step with a Km = 0.2% 02. The oxidative step appears to be after ethylene application, the rate of DNA synthesis from preceded by an energy-requiring step subsequent to me- [3H]thymidine begins to decline not only in the apical meri- thionine formation. stem (Fig. 1; ref. 5), but also even in the elongating zone of Early observations on the effects of ethylene on plant growth the stem where no cell divisions occur (Fig. 2; ref. 5). RNA are contained in a literature, dating to 1858 (1), that describes synthesis from [3H]uridine or [14C]ATP is not affected in the behavior of plants exposed to illuminating gas. In 1901, either tissue (Figs. 1 and 2; ref. 9). DNA synthesis is inhibited the study of a strange growth habit of etiolated pea seedlings because DNA polymerase activity is reduced (10). In roots, raised in laboratory air contaminated with illuminated gas shoots, and lateral buds of the etiolated pea plant there is a revealed that the biologically active component of the gas is quantitative relationship between the inhibitions of DNA ethylene (2). In the presence of ethylene the seedlings undergo synthesis, cell division, and growth caused by ethylene (5). a "triple response," consisting of a thickening of the subapi- Lateral buds are a complex case. After the buds are re- cal portion of the stem, depression in the rate of elongation, leased from apical dominance by removal of the stem apex, and horizontal nutation of the stem. These and numerous their mitotic activity and outgrowth are repressed by applica- other changes in the growth and development of seedlings tion of either ethylene, or enough auxin to induce ethylene might have received immediate attention had not it been production (11, 12). Inclusion of a cytokinin overcomes the learned soon thereafter that ethylene ripens fruits (3). Almost inhibitory action of ethylene or auxin (11-13), but whether all effort was diverted to this economically important aspect this is the manner in which auxin and cytokinin normally of ethylene action, and by the mid-1930s it was established control apical dominance is not resolved. A puzzling thing that ethylene is produced autocatalytically just in advance about ethylene and bud growth is the fact that often apical of fruit ripening (4). The gas became known as the fruit- dominance is broken after an ethylene treatment even though ripening hormone, and not until the early 1960s was the role the gas inhibits the outgrowth of the buds while it is present. No lateral buds grow normally or during a 7-day treatment of Petunia plants with 100 nl/liter of ethylene, but the axillary Abbreviation: 2,4-D, 2,4-dichlorophenoxyacetic acid. buds in the subapical zone of the shoot are released from cor- 591 Downloaded by guest on September 26, 2021 592 Burg Proc. Nat. Acad. Sci. USA 70 (1978) SUBAPEX-INTACT -0-DNA [3H]TWMIDINE --RNA [3HIURIDINE a 6 0 < F IJ 0 2 0 O 0- 4 8 12 16 20 24 HOURS PRETREATMENT WITH 100 tbI/LITER OF C2H4 FIG. 2. Same as Fig. 1, except the subapical 5-mm elongating zone was excised and pulse-labeled with isotope (Kang and Burg, 1972). dominance. In Petunia the effect of applied ethylene on apical C2H4 dominance is quantitatively almost as great as that of excising the apex. A similar mechanism may underlie the breaking of FIG. 1. Effect of ethylene (100 nl/liter) applied to intact dormancy in root initials, buds, seeds, and tubors (14-16) etiolated pea seedlings (7-days old) on the rate of incorporation after brief ethylene treatment. of ['H]thymidine into DNA and [3Hjuridine into RNA. After Several hours after ethylene application, the capacity of the the seedlings were exposed to ethylene for the indicated number of polar auxin transport system begins to decline (17, 18), and hours, either the hook elbow or the apical tip and plumular leaves within 10 hr it is inhibited almost 90% in pea subapical stem were excised and pulse-labeled with a solution containing 1 ,ACi/ml of thymidine or uridine and 50 mM potassium phosphate tissue. As a result, the auxin content of the stem is lowered buffer (pH 7). DNA and RNA were extracted, and isolated; radio- markedly (19-21), possibly in part because auxin synthesis activity was determined. The results were the same regardless of also may be curtailed by ethylene (22). The cause of the block- whether ethylene was present or absent during the pulse-labeling age of auxin transport is not known, but is not enhanced period (Kang and Burg, 1972). i A, hook; O-O, apex-ex- auxin destruction (2, 23) or conjugation (24). In this manner periment 1; *-- , apex-experiment 2. the auxin content of the stem is diminished just as if the natural source of auxin, the apex, had been removed, and it is perhaps for this reason that apical dominance is broken in relative inhibition if the gas is applied for only 2 hr and then some plants when an ethylene treatment is terminated. Other removed (Table 1). When ethylene is removed after an 8- to symptoms of auxin deficiency would be expected and have 12-hr treatment essentially all buds are released from apical been observed when ethylene is applied. This explains in part how the gas causes the abscission of leaves, flowers, and fruits TABLE 1. Ethylene-induced release of apical dominance in (17, 25, 26) for auxin has the opposite effect. Both auxin and 5-week-old Petunia x hybrid Grandiflora calypso seedlings ethylene have been implicated as natural regulators of the (Ramos and Burg, 1972) abscission process (27, 28). % Buds released from apical dominance Effect of ethylene on cell expansion The overall elongation rate of several intact seedlings, includ- Duration of at indicated time (days) etiolated pea, is inhibited by ethylene within 15 C2H4 treatment 2 4 5 7 ing strongly min (Fig. 3; refs. 19, 29, 30). Inhibition of cell expansion is not 2Hr 0 0 9 18 complete in the growing zone of pea. Instead, in the 4 Hr 0 10 13 23 presence of ethylene, the cells continue to expand, albeit 6 Hr 0 15 30 36 slowly, in an isodiametric manner for a seemingly indefinite 8 Hr 4 27 33 37 time, whereas the same cells in control plants differentiate 12 Hr 7 36 36 43 24 Hr 3 43 46 46 within a few days (6, 31).
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