Ethylene accumulation in waterlogged Rumex plants promotes formation of adventitious roots

Accumulation of the gaseous plant hormone ethylene is very importantfor the induction of several responses of plants to flooding.However, little is known about the role of this gas in the formationof flooding-induced adventitious roots. Formation of adventitiousroots in Rumex species is an adaptation of these plants to floodedsoil conditions. The large air-spaces in these roots enablesdiffusion of gases between shoot and roots. Application of ethylene to non-flooded Rumex plants resultedin the formation of adventitious roots. In R. palustris Sm.shoot elongation and epinasty were also observed. The numberof roots in R. thyrsiflorus Fingerh. was much lower than inR. palustris, which corresponds with the inherent differencein root forming capacity between these two species. Ethyleneconcentrations of 1.5–2µI I_{– 1} induced a maximumnumber of roots in both species. Quantification of ethylene escaping from root systems of Rumexplants that were de-submerged after a 24 h submergence periodshowed that average ethylene concentrations in submerged rootsreached 1.8 and 9.1 µl I_–1 in R. palustris and R.thyrsiflorus, respectively. Inhibition of ethylene productionin R. palustris by L--(2-aminoethoxyvinyl)-glycine (AVG) or-aminobutyric acid (AIB) decreased the number of adventitiousroots induced by flooding, indicating that high ethylene concentrationsmay be a prerequisite for the flooding-induced formation ofadventitious roots in Rumex species. Key words: Adventitious roots, epinasty, ethylene, flooding, Rumex, shoot elongation     

Ethylene enhances gibberellin levels and petiole sensitivity in flooding-tolerant Rumex palustris but not in flooding-intolerant R. acetosa

The role of gibberellin (GA) and ethylene in submergence-induced petiole elongation was studied in two species of the genus Rumex. Analysis of endogenous GAs in the flooding-tolerant Rumex palustris Sm. and the intolerant Rumex acetosa L. by gas chromatography-mass spectrometry showed for both species the presence of GA₁, GA₄, GA₉, GA₁₉, GA₂₀ and GA₅₃. Gas chromatography-mass spectrometry analysis of R. palustris petiole tissue of submerged plants showed an increase in levels of 13-OH GAs, especially GA₁, compared with drained plants. This effect could be mimicked by application of 5 μL L⁻¹ ethylene. In R. acetosa, no differences between levels of GAs in drained or submerged plants were found. In R. palustris, both submergence and ethylene treatment sensitized petioles to exogenous gibberellic acid (GA₃). In R. acetosa the effect was opposite, i.e. submergence and ethylene de-sensitized petioles to GA₃. Our results demonstrate the dual effect of ethylene in the submergence response related to flooding tolerance, i.e. in the flooding-tolerant R. palustris ethylene causes an increased concentration of and sensitivity to GA with respect to petiole elongation while in the intolerant R. acetosa ethylene reduces growth independent of GAs. Received: 5 November 1996 / Accepted: 8 February 1997     

Sensitivity to ethylene: the key factor in submergence-induced shoot elongation of Rumex

Rosettes of flooding-resistant Rumex palustris plants show a submergence-induced stimulation of elongation, which is confined to the petioles of young leaves. This response increases the probability of survival. It is induced by ethylene that accumulates in submerged tissues. Flooding-intolerant Rumex acetosella plants do not show this response. We investigated whether differences in shoot elongation between the species, between old and young leaves and between the petiole and leaf blade of a R. palustris plant result from differences in internal ethylene concentration or in sensitivity to the gas. Concentrations of free and conjugated ACC in petioles and leaf blades of R. palustris indicated that ethylene is synthesized throughout the submerged shoot, although production rates varied locally. Nevertheless, no differences in ethylene concentration were found between submerged leaves of various ages. In contrast, dose-response curves showed that only elongation of young petioles of R. palustris was sensitive to ethylene. In R. acetosella, elongation of all leaves was insensitive to ethylene. We conclude that variation in ethylene sensitivity rather than content explains the differences in submergence-induced shoot elongation between the two Rumex species and between leaves of R. palustris.     

Growth and development ofRumex roots as affected by hypoxic and anoxic conditions

The growth characteristics of threeRumex species were determined under different solution oxygen concentrations in hydroculture. These species all occur in a river foreland ecosystem and they were found to differ in their flood tolerance. The flood-tolerantR. maritimus undR. crispus developed a large number of new, aerenchymatous roots within a short period under low solution oxygen concentrations. Biomass production was not affected. In the flood-intolerantR. thyrsiflorus, however, only few slow-growing new roots were developed and biomass production was significantly reduced at solution oxygen concentrations below 2% (v:v). These different responses could be partly explained by a differential aerenchyma formation in new roots of the flood-tolerant species. Aerenchyma can relieve the oxygen stress of the root systems via internal aeration.The fast development of new roots of the flood-tolerantR. maritimus andR. crispus after the onset of anaerobiosis coincided with the reduction or cessation of growth of the primary roots. Notwithstanding the cessation of growth, however, primary roots of both species were able to recover following restoration of aerobic conditions after a 13-day anaerobic period. However, the roots ofR. thyrsiflorus ceased growing very soon after the onset of anaerobiosis. All had died within 10 days.The balance between the growth rates of the primary and the newly formed root system are discussed and related to the differential tolerance of theRumex species to transient flooding.     

Changes in growth,porosity, and radial oxygen loss from adventitious roots of selected mono‐ and dicotyledonous wetland species with contrasting types of aerenchyma

Growth in stagnant, oxygen‐deficient nutrient solution increased porosity in adventitious roots of two monocotyledonous (Carex acuta and Juncus effusus) and three dicotyledonous species (Caltha palustris, Ranunculus sceleratus and Rumex palustris) wetland species from 10 to 30% under aerated conditions to 20–45%. The spatial patterns of radial oxygen loss (ROL), determined with root‐sleeving oxygen electrodes, indicated a strong constitutive ‘barrier’ to ROL in the basal root zones of the two monocotyledonous species. In contrast, roots of the dicotyledonous species showed no significant ‘barrier’ to ROL when grown in aerated solution, and only a partial ‘barrier’ when grown in stagnant conditions. This partial ‘barrier’ was strongest in C. palustris, so that ROL from basal zones of roots of R. sceleratus and R. palustris was substantial when compared to the monocotyledonous species. ROL from the basal zones would decrease longitudinal diffusion of oxygen to the root apex, and therefore limit the maximum penetration depth of these roots into anaerobic soil. Further studies of a larger number of dicotyledonous wetland species from a range of substrates are required to elucidate the ecophysiological consequences of developing a partial, rather than a strong, ‘barrier’ to ROL.     

Internal oxygen transport inRumex species and its significance for respiration under hypoxic conditions

Rumex thyrsiflorus, Rumex crispus andRumex maritimus show a differential flood-tolerance in the river ecosystem in the Netherlands.R. thyrsiflorus occurs at high-elevated habitats and is flood-intolerant, the other two species occur at lower-elevated habitats and are flood-tolerant. We compared their respiratory activity under aerobic and anaerobic conditions in the root environment and quantified the internal gas transport. The results indicate that aerial oxygen can be used for root respiration in both aerobically and anaerobically grown plants. The amount of oxygen used via internal aeration increased with decreasing oxygen concentration in the root environment. Aerobically grown plants ofR. maritimus andR. crispus already showed a high internal aeration, but there was a significant increase in internal oxygen transport in anaerobic plants, where new, aerenchymatous roots had formed. This indicates the functional significance of new root formation for respiration in these species upon hypoxia. After two weeks of anaerobiosis, more than 50% of the total respiration of the roots of young plants ofR. maritumus and 40% of roots of young plants ofR. crispus was due to internal aeration at low oxygen concentrations in the root environment. InR. maritimus both young and old plants performed in this way, inR. crispus only young plants, whileR. thyrsiflorus showed some internal aeration, but this was hardly detectable. These differences can be explained on the basis of a different morphology and concomitant diffusive resistance of both root and shoot system. In experiments with different submergence levels of the shoot, the amount of internal aeration was positively correlated to the total leaf area protruding above the water surface inR. maritimus. This indicates a functional significance of the petiole and leaf elongation response upon total submergence of this species.     

Adaptations to Flooding Stress: From Plant Community to Molecule

Abstract: This review highlights four major topics in plant flooding research: the processes underlying vegetation zonation in the floodplain, the challenges of using model species to reveal adaptive responses in shoots and roots, the role of micro-organisms in flooded soils in relation to plant growth, and the molecular regulation of the hormone ethylene which is heavily involved in the adaptation reaction of flood-resistant plants. Model species and vegetation strategies are used to unravel mechanisms of vegetation zonation in the river flood-plain. In the case of woodlands, hydrological conditions determine to a large extent their zonation patterns under natural conditions. For softwood species, such as Salicaceae, the interaction between water levels and timing of seed dispersal is the dominating process determining their establishment success on river banks. Their strategy is well adapted to irregular, high and prolonged floods. Hardwood species, Quercus, Fraxinus, UImus and Acer, are flood-sensitive and inhabit the higher sites. They mainly have heavy seeds and germinate under shaded conditions. The most shade-tolerant hardwood species are the least well adapted to flooding. Anthropogenically influenced parts of the floodplain are characterized by grasslands with elevation level and management practices determining the species composition. Low-lying grasslands have flood-tolerant species; elevated zones are seldom flooded and have flooding-sensitive species. Following Grime (1998^[59]), plant species of major vegetation types within the floodplain zone can be divided into three categories–dominants, subordinates and transients–illustrating the diversity in plant species in relation to environmental properties. Model species that are indicative of the different conditions in the various zones are chosen to help in the understanding of morphological and physiological adaptations at the plant level. The formation of aerenchymatous roots and the capacity to elongate shoot parts upon submergence are among the main responses of surviving plants. The role of hormones in the adaptation reaction is emphasized. Owing to high porosities in roots of flood-tolerant plants, radial oxygen loss greatly influences nitrification and denitrification processes in the flooded soil. Nutrient cycles are restored by root-derived oxygen and the oxygenated rhizosphere is detoxified. A new development in flooding ecology is the unravelling of the molecular regulation of hormonally controlled processes. The expression of an ethylene receptor gene in Rumex palustris is highlighted. This paper ends with some suggestions for future flooding research.     

Effect of auxin and ethylene on elongation of intact primary roots of maize (Zeamays L.)

We tested that the hypothesis that root elongation might be controlled by altering the level of ethylene in intact primary roots of maize(Zea mays L.). We measured root elongation in a short period using a computerized root auxanometer. Compounds which regulate ethylene production were applied to intact primary roots in different time periods. Root elongation was stimulated by the treatment with ethylene antagonists such as Co²⁺, aminoethoxyvinylglycine (AVG) and L-canaline. This result suggested that root elongation was closely related to ethylene level of intact primary roots. Furthermore, IAA- and 1-aminocyclopropane-1-carboxylic acid (ACC)-induced inhibition of root elongation was reversed by treatment with Co²⁺. The application of ACC to roots which have been exposed to IAA and Co²⁺ have no significant effect on root elongation. However, the inhibition of root elongation by ACC in roots previously treated with IAA and AVG became manifest when the applied IAA concentrations were lower. These results were consistent with the hypothesis that the level of ethylene in intact roots functions to moderate root elongation, and suggested that auxin-induced inhibition of root elongation results from auxin induced promotion of ethylene production.     

Effect of ethylene antagonists on auxin-induced inhibition of intact primary root elongation in maize (Zeamays L.)

We tested that the hypothesis that root elongation might be controlled by altering the level of ethylene in intact primary roots of maize(Zea mays L.). We measured root elongation in a short period using a computerized root auxanometer. Compounds which regulate ethylene production were applied to intact primary roots in different time periods. Root elongation was stimulated by the treatment with ethylene antagonists such as Co²⁺, aminoethoxyvinylglycine (AVG) and L-canaline. This result suggested that root elongation was closely related to ethylene level of intact primary roots. Furthermore, IAA- and 1-aminocyclopropane-1-carboxylic acid (ACC)-induced inhibition of root elongation was reversed by treatment with Co²⁺. The application of ACC to roots which have been exposed to IAA and Co²⁺ have no significant effect on root elongation. However, the inhibition of root elongation by ACC in roots previously treated with IAA and AVG became manifest when the applied IAA concentrations were lower. These results were consistent with the hypothesis that the level of ethylene in intact roots functions to moderate root elongation, and suggested that auxin-induced inhibition of root elongation results from auxin induced promotion of ethylene production.