Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen

Abstract

Adventitious roots of two to four-weekold intact plants of Zea mays L. (cv. LG11) were shorter but less dense after extending into stagnant, non-aerated nutrient solution than into solution continuously aerated with air. Dissolved oxygen in the non-aerated solutions decreased from 21 kPa to 3-9 kPa within 24 h. When oxygen partial pressures similar to those found in non-aerated solutions (3, 5 and 12 kPa) were applied for 7 d to root systems growing in vigorously bubbled solutions, the volume of gas-space in the cortex (aerenchyma) was increased several fold. This stimulation of aerenchyma was associated with faster ethylene production by 45-mm-long apical root segments. When ethylene production by roots exposed to 5 kPa oxygen was inhibited by aminoethoxyvinylglycine (AVG) dissolved in the nutrient solution, aerenchyma formation was also retarded. The effect of AVG was reversible by concomitant applications of 1-aminocyclopropane-1-carboxylic acid, an immediate precursor of ethylene. Addition of silver nitrate, an inhibitor of ethylene action, to the nutrient solution also prevented the development of aerenchyma in roots given 5 kPa oxygen. Treating roots with only 1 kPa oxygen stimulated ethylene production but failed to promote gas-space formation. These severely oxygen-deficient roots seemed insensitive to the ethylene produced since a supplement of exogeneous ethylene that promoted aerenchyma development in nutrient solution aerated with air (21 kPa oxygen) failed to do so in nutrient solution supplied with 1 kPa oxygen. Both ethylene production and aerenchyma formation were almost completely halted when roots were exposed to nutrient solutions devoid of oxygen. Thus both processes require oxygen and are stimulated by oxygen-deficient surroundings in the 3-to 12-kPa range of oxygen partial pressures when compared with rates observed in air (21 kPa oxygen).

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

“…Levels of ACC and rates of ethylene production in our control roots were similar to previously published values for maize root tips (2,11,18). The response to nutrient deprivation therefore contrasts sharply with that to oxygen deficiency (hypoxia).…”

“…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. 2), as well as the action of the inhibitor of ACC synthase (AVG) (18,21) to assume that essentially the same pathway from methionine to ethylene is followed in maize roots as in many other plant tissues especially fruits that have been more fully described (14,15,26,31). The present results can therefore be examined in relation to what is known concerning the regulation of this pathway in other plant tissues.…”

“…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).However, Konings and Verschuren (21) showed that formation of aerenchyma in the seminal roots of maize was stimulated under fully aerobic conditions by omission of either a nitrogen source (nitrate or ammonium) or phosphate. Similar results were obtained with the adventitious roots of another maize variety (13), while omission ofpotassium under similar conditions did not induce aerenchyma.…”

Acclimation to soil flooding — sensing and signal-transduction

“…One would expect that accumulation of ethylene due to the physical entrapment by the surrounding water-saturated soil suffices to induce aerenchyma. Nevertheless, the prevalent low oxygen concentrations further stimulate ethylene production (Jackson et al, 1985a), thereby adding to the build-up of ethylene concentrations. Ethylene levels exceeding 0.5 µL L −1 are usually sufficient to evoke the maximum response in treated roots.…”

Induction of Enzymes Associated with Lysigenous Aerenchyma Formation in Roots of Zea mays during Hypoxia or Nitrogen Starvation

“…With hypoxia, ethylene biosynthesis is accelerated, endogenous concentrations increase, and application of low concentrations of ethylene (1 pL L-' ethylene in air) stimulates aerenchyma formation in well-aerated, complete nutrient solution (Drew et al, 1979;Jackson et al, 1985;Atwell et al, 1988). Inhibitors of ethylene action (Ag+) or biosynthesis (AVG) effectively block aerenchyma formation in hypoxic roots (Drew et al, 1981;Konings, 1982;Jackson et al, 1985). However, whereas hypoxia stimulates ethylene production, N or P deficiency Supported by U.S. Department of Agriculture Competitive Grant NO.…”