Benefits of flooding-induced aquatic adventitious roots depend on the duration of submergence: linking plant performance to root functioning

Abstract

Background and aims: Temporal flooding is a common environmental stress for terrestrial plants. Aquatic adventitious roots (aquatic roots) are commonly formed in flooding-tolerant plant species and are generally assumed to be beneficial for plant growth by supporting water and nutrient uptake during partial flooding. However, the actual contribution of these roots to plant performance under flooding has hardly been quantified. As the investment into aquatic root development in terms of carbohydrates may be costly, these costs may - depending on the specific environmental conditions - offset the beneficial effects of aquatic roots. This study tested the hypothesis that the balance between potential costs and benefits depends on the duration of flooding, as the benefits are expected to outweigh the costs in long-term but not in short-term flooding.

Methods: The contribution of aquatic roots to plant performance was tested in Solanum dulcamara during 1-4 weeks of partial submergence and by experimentally manipulating root production. Nutrient uptake by aquatic roots, transpiration and photosynthesis were measured in plants differing in aquatic root development to assess the specific function of these roots.

Key results: As predicted, flooded plants benefited from the presence of aquatic roots. The results showed that this was probably due to the contribution of roots to resource uptake. However, these beneficial effects were only present in long-term but not in short-term flooding. This relationship could be explained by the correlation between nutrient uptake and the flooding duration-dependent size of the aquatic root system.

Conclusions: The results indicate that aquatic root formation is likely to be selected for in habitats characterized by long-term flooding. This study also revealed only limited costs associated with adventitious root formation, which may explain the maintenance of the ability to produce aquatic roots in habitats characterized by very rare or short flooding events.

Keywords: Adventitious root removal; Solanum dulcamara; benefit; cost; flooding duration; nutrient uptake; partial submergence; plasticity; root function; water uptake.

Fig. 1.

Relationship between the dry weight of aquatic adventitious roots and the total dry weight (adventitious root dry weight excluded) of the entire plant after 3 weeks of experimental partial flooding in plants originating from dry (open symbols) and wet (shaded symbols) habitats along the Dutch coast (original data from Zhang et al., 2016). To test the relationship between adventitious root dry weight with total plant dry weight excluding adventitious root dry weight across 18 populations of S. dulcamara (Zhang et al., 2016), a linear regression model was fitted with adventitious root dry weight and the total plant dry weight as independent and dependent variables, respectively.

Fig. 2.

Mean (± 1 s.e.) shoot and root (aquatic adventitious roots and non-adventitious sediment roots) dry weight (A), stem height (B) and leaf size (C) after 3 weeks of drained or partially flooded conditions, and control treatment (no primordia removal), Vaseline treatment (where the lower stem parts including the root primordia were covered with Vaseline), removal of adventitious root primordia, or wounding treatment (where similar wounds as with primordia removal were made on the stem without damaging the primordia), respectively. Significant differences among treatments within drained or flooded conditions are indicated with different letters (P < 0·05, n = 11).

Fig. 3.

Correlation between total surface area of the aquatic adventitious roots of S. dulcamara and the uptake rates of phosphate under partially flooded conditions. The uptake rate was calculated after 6 h of incubation of the adventitious roots in a closed cuvette that was fixed around the stem and contained nutrient solution. Slopes, correlation coefficients and statistical significance of the linear regression line are indicated.

Fig. 4.

Mean (± 1 s.e.) rates and ANOVA results of leaf transpiration (A), photosynthesis (B) and stomatal conductance (C) of plants in partial submergence treatments (With ARs: plants were able to maintain aquatic adventitious roots during flooding; Without ARs: plants were not able to produce aquatic adventitious roots due to full coverage of Vaseline on the flooded stem). The mean (± 1 s.e.) rates of leaf transpiration, stomatal conductance and photosynthesis of plants under drained conditions were 1·10 (± 0·22), 0·13 (± 0·026) and 7·86 (± 1·05) (all units as given in the body of the figure), respectively. The significance levels were *0·01 < P < 0·05, ^$0·05 < P < 0·1.

Fig. 5.

Mean (± 1 s.e.) aquatic adventitious root dry weight (A) and number (B) of S. dulcamara plants after 1, 2 and 4 weeks of partial submergence, respectively, and scanning image of an individual main adventitious root including lateral roots (C) after 3 weeks of partial submergence. Significant differences are indicated with different letters (P < 0·05 after Bonferroni correction for pairwise t test in R, n = 6–8).

Fig. 6.

Mean (± 1 s.e.) total dry weight (A), sediment root dry weight (B), stem height (C) and leaf size (D) for plants with aquatic adventitious roots (ARs) and without ARs after 1, 2 and 4 weeks of partial submergence, respectively. Significant effects of aquatic adventitious root removal within each submergence duration are indicated by asterisks, ***P < 0·0003, **0·0003 < P < 0·003, *0·003 < P < 0·002 (P values were adjusted by Bonferroni correction, n = 6–8).