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. 2016 Oct 1;118(4):675-683.
doi: 10.1093/aob/mcw051.

Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants

Affiliations

Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants

Qiaoli Ayi et al. Ann Bot. .

Abstract

Background and Aims Flooding imposes stress upon terrestrial plants because it results in oxygen deficiency, which is considered a major problem for submerged plants. A common response of terrestrial plants to flooding is the formation of aquatic adventitious roots. Some studies have shown that adventitious roots on submerged plants are capable of absorbing water and nutrients. However, there is no experimental evidence for the possible oxygen uptake function of adventitious roots or for how important this function might be for the survival of plants during prolonged submergence. This study aims to investigate whether adventitious roots absorb oxygen from the water column, and whether this new function is beneficial to the survival of completely submerged plants. Methods Taking Alternanthera philoxeroides (Mart.) Griseb. as a representative species, the profiling of the underwater oxygen gradient towards living and dead adventitious roots on completely submerged plants was conducted, the oxygen concentration in stem nodes with and without adventitious roots was measured, and the growth, survival and non-structural carbohydrate content of completely submerged plants with and without adventitious roots was investigated. Key Results Oxygen profiles in the water column of adventitious roots showed that adventitious roots absorbed oxygen from water. It is found that the oxygen concentration in stem nodes having adventitious roots was higher than that in stem nodes without adventitious roots, which implies that the oxygen absorbed by adventitious roots from water was subsequently transported from the roots to other plant tissues. Compared with plants whose adventitious roots had been pruned, those with intact adventitious roots had slower leaf shedding, slower plant mass reduction, more efficient carbohydrate economy and prolonged survival when completely submerged. Conclusions The adventitious roots of A. philoxeroides formed upon submergence can absorb oxygen from ambient water, thereby alleviating the adverse effects of oxygen deficiency, enabling efficient utilization of carbohydrates and delaying the death of completely submerged plants.

Keywords: Alternanthera philoxeroides (Mart.) Griseb.; aquatic adventitious roots; microelectrode; oxygen uptake; submergence tolerance.

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Figures

Fig. 1.
Fig. 1.
Schematic representation of the experimental set-up for profiling of the oxygen gradient towards an adventitious root surface under water. The plant with adventitious roots was placed at the bottom of the water tank and the target adventitious root was fixed onto the background board. The whole potted Alternanthera philoxeroides plant was submerged with air-saturated water for about 1 h. The microelectrode was fixed on a micromanipulator, and used to measure the underwater oxygen profile over a distance of approx. 1200 μm by advancing a step of 50 μm every 5 s, moving towards the root surface.
Fig. 2.
Fig. 2.
Oxygen profiles in the water column adjacent to (A) living adventitious roots (n = 4), (B) dead adventitious roots (n = 3) and (C) the background board without roots (n = 4) in darkness at 25 °C. Values are given as the mean ± s.e. By using an O2 microelectrode (tip diameter 10 μm), underwater profiling was conducted towards a point of the adventitious root; the point was approx. 10 mm away from the point of attachment of the adventitious root to the stem of Alternanthera philoxeroides.
Fig. 3.
Fig. 3.
O2 concentration (mean ± s.e., n = 3) in stem nodes with or without adventitious roots in darkness at 25 °C under complete submergence. During the measurement, Alternanthera philoxeroides plants were completely submerged to a depth of 15 cm. An asterisk indicates a significant difference at P < 0·05 between treatments (unpaired t-test).
Fig. 4.
Fig. 4.
Indicators of plant vitality. Dynamics of leaf shedding (A) and stem apical tissue vitality (B) of Alternanthera philoxeroides plants with and without adventitious roots during complete submergence in darkness at 25 °C. In (A), values are given as the mean ± s.e. (n = 17) and an asterisk indicates that the number of leaves on plants between the two treatments was significantly different (P < 0·05, unpaired t-test) on the last day of recording. In (B), the pruning of adventitious roots had negative effects on the stem apical tissue vitality of plants at final harvest. (χ2 test, d.f. = 1, χ2 = 4·246, P = 0·039; 17 plants used in each treatment).
Fig. 5.
Fig. 5.
Relative growth rate (RGR) (g g–1 d–1) (means ± s.e., n = 17) of dry mass (A) and leaf area ratio (LAR) (B) of Alternanthera philoxeroides plants with and without adventitious roots after 38 d complete submergence in darkness at 25 °C. Asterisk indicates significant differences between the two treatments (P < 0·05, unpaired t-test).
Fig. 6.
Fig. 6.
Content (means ± s.e.) of non-structural carbohydrates (including starch and soluble sugars) in leaves (A) and stems (B) of completely submerged Alternanthera philoxeroides plants with and without adventitious roots. For either soluble sugars or starch, different letters indicate a significant difference (P < 0·05) between treatments. Stem non-structural carbohydrate contents were determined with 20 replicates each for plants with and without adventitious roots; leaf non-structural carbohydrate contents were determined with eight replicates for plants with adventitious roots and six replicates for plants without adventitious roots.

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