Inhibition of Ethylene Synthesis in Tomato Plants Subjected to Anaerobic Root Stress

Abstract

Enhanced ethylene production and leaf epinasty are characteristic responses of tomato (Lycopersicon escukntum Mill.) to waterlogging. It has been proposed (Bradford, Yang 1980 Plant Physiol 65: 322-326) that this results from the synthesis of the immediate precursor of ethylene, 1-aminocyclopropane-I-carboxylic acid (ACC), in the waterlogged roots, its export in the transpiration stream to the shoot, and its rapid conversion to ethylene. Inhibitors of the ethylene biosynthetic pathway are available for further testing of this ACC transport hypothesis: aminooxyacetic acid (AOA) or aminoethoxyvinylglycine (AVG) block the synthesis of ACC, whereas CO2 prevents its conversion to ethylene. AOA and AVG, supplied in the nutrient solution, were found to inhibit the synthesis and export of ACC from anaerobic roots, whereas Co2" had no effect, as predicted from their respective sites of action. Transport of the inhibitors to the shoot was demonstrated by their ability to block wound ethylene synthesis in excised petioles. Al three inhibitors reduced petiolar ethylene production and epinasty in anaerobically stressed tomato plants. With AOA and AVG, this was due to the prevention of ACC import from the roots as well as inhibition of ACC synthesis in the petioles. With Co21, conversion of both root-and petiole-synthesized ACC to ethylene was blocked. Collectively, these data support the hypothesis that the export of ACC from low 02 roots to the shoot is an important factor in the ethylene physiology of waterlogged tomato plants.Ethylene is an important endogenous regulator of plant responses to waterlogging (7,14). Under the low 02 conditions in the soil during flooding, tomato roots synthesize ACC,3 the immediate precursor of ethylene, and transport it in the xylem to the shoot, where it is rapidly converted to ethylene (8,9). This increase in the ethylene content of the shoot tissues results in petiole epinasty, aerenchyma formation, and other anatomical and morphological responses associated with waterlogging (6,11,14).The sites of inhibition in the biosynthetic pathway of ethylene are now known for several inhibitors. Application of these inhibitors allows further tests of the role of root-synthesized ACC in shoot responses to waterlogging. AOA and AVG effectively prevent the conversion of SAM to ACC, both in vivo (1,22,23) conversion of ACC to ethlene. Co2" on the other hand, has no effect on ACC synthesis but inhibits the formation of ethylene from ACC (23). These compounds, therefore, permit inhibition of ethylene biosynthesis at specific steps in the pathway (see 18, 19, for reviews). In waterlogged plants, the locations of stress-induced ACC synthesis and its conversion to ethylene are separated spatially, with the formation of ACC from SAM occurring in the roots and conversion of ACC to ethylene occurring in the shoot.Thus, the effects of application of AOA, AVG, or Co2" to anaerobic roots should reflect their differing sites of action. In this study, these inhibitors were used to further characterize th...

Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.

“…In maize (2), ethylene production rates as well as ACC concentration were raised many-fold in the roots when in nutrient solution sparged with 5% (v/v) oxygen in nitrogen (about one-quarter the oxygen concentration in air). Flooding of the root system in tomato strongly stimulated production of ACC by roots and its transport in the transpiration stream to shoots (4,5). Likewise, in the hypoxic intemodes of submerged, deep water rice, promotion of ethylene synthesis was accompanied by enhancement of ACC synthase activity (7, Although not all the components of the ethylene biosynthetic pathway have been examined in maize roots, there is sufficient information from characterization of ACC, ACC synthase, and EFE (this paper and ref.…”

“…In earlier reports we showed that aerenchyma formation in adventitious (nodal) roots of maize by cell lysis is induced by a partial oxygen deficiency (hypoxia) and is closely related to enhanced endogenous concentrations of ethylene (1 1). Hypoxia clearly stimulates the biosynthesis of ethylene in growing maize roots (2,11,12,20) as in other responsive plant tissues (4,5,7). Low exogenous concentrations of ethylene under aerobic conditions (1-5 uL L-' in air) induce aerenchyma (18) that is structurally indistinguishable from that induced by hypoxia (1 1, 12); furthermore, hypoxically induced aerenchyma formation in the apices of growing roots is blocked by inhibitors of ethylene biosynthesis or ethylene action (12,18,20).…”

1-Aminocyclopropane-1-Carboxylic Acid Transported from Roots to Shoots Promotes Leaf Abscission in Cleopatra Mandarin (Citrus reshni Hort. ex Tan.) Seedlings Rehydrated after Water Stress

“…Roots were placed into the pressure chamber cylinder with the cut end out of the cylinder. A plastic tube was connected to the cut end to collect xylem fluid and a pressure of 2 MPa was applied for 5 min. Approximately 250 uL of fluid were obtained from rehydrated plants.…”

“…Ethylene is the natural regulator of abscission, and due to its gaseous nature, it may be that this abscission-inducing factor is ACC, the metabolic precursor of ethylene. Xylem transport of ACC from roots to shoots was first demonstrated by Bradford and Yang to induce epinasty in tomato plants subjected to anaerobic root stress (5,6). Later, interorgan ACC transport was shown in several systems (3,9,12,18,21,23,28,29).…”

Enhanced chickpea growth-promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene

“…In addition, ethylene levels are increased in the shoots of waterlogged plants, and its accumulation is responsible for the development of the waterlogging symptoms including epinasty and chlorosis (Vartapetian and Jackson 1997). The high production and accumulation of ethylene in shoots results from the high ACC levels, synthesized in roots by ACC synthase, then transported from the root system to shoot where it is converted to ethylene by ACC oxidase (Bradford et al 1982). Since oxygen concentrations of waterlogged root systems are too low or nonexistent, the conversion of ACC to ethylene by ACC oxidase cannot take place (Jackson and Campbell 1976;Bradford and Dilley 1978;Wang and Arteca 1992;Banga et al 1997).…”