Effects of Ethylene on the Kinetics of Curvature and Auxin Redistribution in Gravistimulated Roots of Zea mays

Abstract

We tested the involvement of ethylene in maize (Zea mays L.) root gravitropism by measuring the kinetics of curvature and lateral auxin movement in roots treated with ethylene, inhibitors of ethylene synthesis, or inhibitors of ethylene action. In the presence of ethylene the latent period of gravitropic curvature appeared to be increased somewhat. However, ethylene-treated roots continued to curve after control roots had reached their final angle of curvature. Consequently, maximum curvature in the presence of ethylene was much greater in ethylene-treated roots than in controls. Inhibitors of ethylene biosynthesis or action had effects on the kinetics of curvature opposite to that of ethylene, i.e. the latent period appeared to be shortened somewhat while total curvature was reduced relative to that of controls. Label from applied 3H-indole-3-acetic acid was preferentially transported toward the lower side of stimulated roots. In parallel with effects on curvature, ethylene treatment delayed the development of gravity-induced asymmetric auxin movement across the root but extended its duration once initiated. The auxin transport inhibitor, 1-N-naphthylphthalamic acid reduced both gravitropic curvature and the effect of ethylene on curvature. Since neither ethylene nor inhibitors of ethylene biosynthesis or action prevented curvature, we conclude that ethylene does not mediate the primary differential growth response causing curvature. Because ethylene affects curvature and auxin transport in parallel, we suggest that ethylene modifies curvature by affecting gravityinduced lateral transport of auxin, perhaps by interfering with adaptation of the auxin transport system to the gravistimulus.The role of ethylene in gravitropism is controversial. Burg and Burg (1) suggested that accumulation of auxin along the lower side of gravistimulated roots leads to enhancement ofethylene production there. They proposed that the elevation of ethylene leads to growth inhibition resulting in downward curvature. This interpretation now seems overly simplified since we now know that root gravitropism results from acceleration of growth along the upper side as well as inhibition along the lower side (9, 15). Also, there is evidence that the elevation of ethylene levels in auxin-treated roots may be insufficient to account for auxin-induced growth inhibition (3). Wheeler and Salisbury (19) reported that inhibitors of ethylene biosynthesis or action retard shoot gravitropism, and they suggested that ethylene mediates gravitropic curvature in these shoots. However, questions have been raised regarding both the statistical significance of the inhibitions observed and the specificity of the high concentrations of inhibitors used in this study (14). Harrison and Pickard (6) studied the role of ethylene in the negative gravitropic response oftomato hypocotyls. They found that gravitropism can occur without substantial changes in ethylene production and also that curvature is unaffected by raising or lowering ethylene in the hypocoty...

Ethylene Modulates Flavonoid Accumulation and Gravitropic Responses in Roots of Arabidopsis

“…If flavonoid expression is under the same light control in maize seedlings as in Arabidopsis seedlings (Wade et al, 2001;Muller et al, 2005), their dark-grown seedlings may mimic our tt4 mutants with an absence of flavonoid synthesis. This complex role of ethylene, with both stimulatory and inhibitory effects on root gravitropism, may explain the contradictory conclusions in the literature on the question of whether ethylene regulates gravitropism (Wheeler and Salisbury, 1981;Kaufman et al, 1985;Harrison and Pickard, 1986;Wheeler et al, 1986;Lee et al, 1990;Woltering, 1991;Kiss et al, 1999;Madlung et al, 1999). Because both ethylene and flavonoid synthesis are regulated by light, nutrients, and other environmental signals (WinkelShirley, 2002;Vandenbussche et al, 2003), it is likely that these contradictory results come from studies in which the synthesis of these molecules is differentially regulated.…”

“…In support of this idea, ethylene reduced polar IAA transport in shoot tissues of several species (Morgan and Gausman, 1966;Suttle, 1988). Additionally, ethylene reduced the lateral redistribution of auxin across gravity-stimulated corn roots (Lee et al, 1990). The agravitropic mutant eir1 is insensitive to ethylene inhibition of root growth and has a defect in a gene encoding a protein linked to auxin efflux (Luschnig et al, 1998).…”

“…A recent study indicated that ethylene increased gravitropic curvature in etiolated maize (Zea mays) roots under conditions where ethylene inhibited elongation (Chang et al, 2004). Several studies reported that low concentrations of ethylene affected the rate of gravitropic curvature, but that the plants ultimately reach the same final angle of orientation in the presence of this gas (Wheeler and Salisbury, 1981;Wheeler et al, 1986;Lee et al, 1990). The absence of kinetic data at the early times after gravitropic stimulation in several of the experiments may explain negative results (Kaufman et al, 1985;Harrison and Pickard, 1986;Woltering, 1991).…”

“…Exogenous applications of ethylene gas or the ethylene precursor 1-aminocyclopropane carboxylic acid (ACC) were used to test the role of ethylene in gravitropic responses in a range of species, with contradictory results. In some experiments, ethylene treatment clearly reduced gravitropic responses (Wheeler and Salisbury, 1981;Wheeler et al, 1986;Lee et al, 1990;Kiss et al, 1999;Madlung et al, 1999), whereas others showed no effects (Kaufman et al, 1985;Harrison and Pickard, 1986;Woltering, 1991). A recent study indicated that ethylene increased gravitropic curvature in etiolated maize (Zea mays) roots under conditions where ethylene inhibited elongation (Chang et al, 2004).…”

The Fast and Transient Transcriptional Network of Gravity and Mechanical Stimulation in the Arabidopsis Root Apex

“…Lateral redistribution of radiolabeled indole-3-acetic acid (IAA) has been measured in both shoots (Parker and Briggs, 1990) and roots (Young et al, 1990;Young and Evans, 1996), and the redistribution of IAA has been shown to precede differential growth (Parker and Briggs, 1990). Other plant hormones, specifically brassinosteroids (Kim et al, 2000), ethylene (Lee et al, 1990;PhilosophHadas et al, 1996;Madlung et al, 1999), cytokinin (Golan et al, 1996), and gibberellic acid (Moore and Dickey, 1985;Rood et al, 1987;Brock and Kaufman, 1988;Chaban et al, 1999) have been shown to also play a role in gravitropism. Reactive oxygen species may function as a downstream component in auxinmediated signal transduction (Joo et al, 2001).…”