Photosynthetic acclimation is important for post-submergence recovery of photosynthesis and growth in two riparian species

Abstract

Background and aims: Concomitant increases in O(2) and irradiance upon de-submergence can cause photoinhibition and photo-oxidative damage to the photosynthetic apparatus of plants. As energy and carbohydrate supply from photosynthesis is needed for growth, it was hypothesized that post-submergence growth recovery may require efficient photosynthetic acclimation to increased O(2) and irradiance to minimize photo-oxidative damage. The hypothesis was tested in two flood-tolerant species: a C(3) herb, Alternanthera philoxeroides; and a C(4) grass, Hemarthria altissima. The impact of low O(2) and low light, typical conditions in turbid floodwater, on post-submergence recovery was assessed by different flooding treatments combined with shading.

Methods: Experiments were conducted during 30 d of flooding (waterlogging or submergence) with or without shading and subsequent recovery of 20 d under growth conditions. Changes in dry mass, number of branches/tillers, and length of the longest internodes and main stems were recorded to characterize growth responses. Photosynthetic parameters (photosystem II efficiency and non-photochemical quenching) were determined in mature leaves based on chlorophyll a fluorescence measurements.

Key results: In both species growth and photosynthesis recovered after the end of the submergence treatment, with recovery of photosynthesis (starting shortly after de-submergence) preceding recovery of growth (pronounced on days 40-50). The effective quantum yield of photosystem II and non-photochemical quenching were diminished during submergence but rapidly increased upon de-submergence. Similar changes were found in all shaded plants, with or without flooding. Submerged plants did not suffer from photoinhibition throughout the recovery period although their growth recovery was retarded.

Conclusions: After sudden de-submergence the C(3) plant A. philoxeroides and the C(4) plant H. altissima were both able to maintain the functionality of the photosynthetic apparatus through rapid acclimation to changing O(2) and light conditions. The ability for photosynthetic acclimation may be essential for adaptation to wetland habitats in which water levels fluctuate.

Fig. 1

Transverse sections of stem/culm (A, B) and root tissues (C, D) of Shaded-submerged plants of A. philoxeroides (A, C) and H. altissima (B, D). Sections were made at 30 mm above and 30 mm below the soil surface for stems/culms and roots, respectively. Note that these tissues were formed during the cultivation before the flooding treatment, not during the flooding treatment. Arrows indicate pith cavity and aerenchyma. Scale bars = 0·2 mm.

Fig. 2

Changes in above-ground dry mass (A, D), below-ground dry mass (B, E) and root-to-shoot ratio (C, F) of A. philoxeroides (A–C) and H. altissima (D–F) following the different flooding treatments with or without shading. Each value is a mean of 8–10 plants (±s.e.). All plants were under the Control condition on day 0. For A. philoxeroides, plants of Shaded-control and Shaded-waterlogged were not harvested on day 40. Different lower-case letters indicate statistically significant differences (P < 0·05 by one-way ANOVA) between the treatments at each time point. Different upper-case letters indicate statistically significant differences (P < 0·05 by the Kruskal–Wallis test) between the measurement time points for each treatment.

Fig. 3

Changes in the total branch/tiller number of A. philoxeroides (A) and H. altissima (B) following the different flooding treatments with or without shading. Each value is a mean of 8–10 plants (±s.e.). All plants were under the Control condition on day 0. Different lower-case letters indicate statistically significant differences (P < 0·05 by one-way ANOVA) between the treatments at each time point. Different upper-case letters indicate statistically significant differences (P < 0·05 by the Kruskal–Wallis test) between the measurement time points for each treatment.

Fig. 4.

Length of the longest internodes (A, C) and the main stem/culm (B, D) for A. philoxeroides (A, B) and H. altissima (C, D) at the end of the different flooding treatments with or without shading. Each value is a mean of 8–10 plants (±s.e.). All plants were under the Control condition on day 0. Different lower-case letters indicate statistically significant differences (P < 0·05 by one-way ANOVA) between the treatments at each time point. Different upper-case letters indicate statistically significant differences (P < 0·05 by the Kruskal–Wallis test) between the measurement time points for each treatment.

Fig. 5.

Changes in the maximal quantum yield of photosystem II (F_v/F_m) in dark-adapted leaves of A. philoxeroides (A, B) and H. altissima (C, D) during and after different flooding treatments with or without shading. Data from Shaded-submerged plants are shown in comparison with Control and Waterlogged plants (A, C) or with Shaded-control and Shaded-waterlogged plants (B, D). Measurements for Shaded-submerged plants were started at the end of the submergence treatment on day 30. Symbols are mean values (±s.e., n = 4–5).

Fig. 6.

Changes in the effective quantum yield of photosystem II (ΔF/F_m′) in leaves of A. philoxeroides (A, B) and H. altissima (C, D) during and after different flooding treatments with or without shading. Values were obtained after 4·5 min of illumination at 800 µmol photons m⁻² s⁻¹. Data from Shaded-submerged plants are shown in comparison with Control and Waterlogged plants (A, C) or with Shaded-control and Shaded-waterlogged plants (B, D). Measurements for Shaded-submerged plants were started at the end of the submergence treatment on day 30. Symbols are mean values (±s.e., n = 4–5).

Fig. 7.

Changes in non-photochemical energy quenching (NPQ) in leaves of A. philoxeroides (A, B) and H. altissima (C, D) during and after different flooding treatments with or without shading. Values were obtained after 4·5 min of illumination at 800 µmol photons m⁻² s⁻¹. Data from Shaded-submerged plants are shown in comparison with Control and Waterlogged plants (A, C) or with Shaded-control and Shaded-waterlogged plants (B, D). Measurements for Shaded-submerged plants were started at the end of the submergence treatment on day 30. Symbols are mean values (±s.e., n = 4–5).