The aim of this study was to improve knowledge on physiological patterns of oak trees' tolerance to waterlogging (or flooding), in order to discriminate useful settings to assess their tolerance potential. In plants the main constraint caused by flooding is the lack of oxygen (root hypoxia) leading to an energy crisis. The responses to this stress were investigated under controlled conditions in two sympatric oak species known to display different ecological requirements, particularly relative to waterlogging. The tolerant pedunculate oak and the more sensitive sessile oak were studied at the early stage of seedling development, in presence of their cotyledons. Potted seedlings were submitted during two flush of growth to a waterlogging or a control treatment. A drainage stage following the waterlogging was included in a third treatment to mimic a temporary soil flooding (most usual cases on the field). One part of the study was related to seedling growth development, especially root distribution. A second part deals with nitrogen nutrition (assimilation and allocation), that was previously assessed by monitoring changes in mineral nitrogen composition of the rhizosphere. Finally, a third part examines the pattern of carbohydrate management (starch and soluble carbohydrates). In both species, the first flush of growth was not inhibited by waterlogging whereas the second flush was severely disrupted, while the root growth was drastically reduced. Nevertheless, pedunculate oak showed a stronger root system than sessile oak, especially by maintaining root colonization in the shallow waterlogged soil layer (adventitious roots). Moreover, pedunculate oak showed the ability to regenerate a strong root system quickly after drainage. The growth recovery of pedunculate oak seedlings was greater than that of sessile oak, allowing its better establishment on hydromorphic soils since the early stage of seedlings. The nitrogen monitoring in the rhizospheric flooded soil showed a switch from nitrate to ammonia, reversible after drainage. The nitrogen metabolism was similar in the two oak species. The key enzymatic activities of the nitrogen assimilation pathway (nitrate reductase and glutamine synthetase) were not clearly affected in the roots neither in the leaves. However, under waterlogging the two oak species showed nitrogen deficiency in the leaves. Overall, nitrogen nutrition is not a feature of waterlogging tolerance which can discriminate these two oak species. The total starch content of waterlogged seedlings was significantly decreased in both species but starch accumulation process remained active, especially in the first flush stem and in the upper taproot section. The overall management of carbohydrates was significantly different between the two oak species when subjected to waterlogging. Under waterlogging, pedunculate oak showed both starch accumulation and a growth rate higher than sessile oak, while carbohydrate mobilization from cotyledons was delayed by waterlogging especially in pedunculate oak seedlings. The α-amylase enzyme activity in cotyledons was corroborated at the rate of starch mobilization. Unlike crop plants (e.g. rice, wheat), tolerance to waterlogging of oak seedlings was not related to higher rates of carbohydrate mobilization from cotyledons. Pedunculate oak seems able to save its carbohydrate reserves until the growth conditions are more favourable and therefore it was able to better sustain a fast and strong recovery after drainage. Over the duration of the experiments, despite a growth limitation, waterlogged seedlings did not seem under carbon limitation because soluble carbohydrate availability was maintained in roots. However, the obtained results showed a carbon imbalance in sessile oak seedlings. Thus, carbon limitation and then carbohydrate starvation could take place. The features of carbohydrate management, related to the whole plant's carbon metabolism, and root growth appear crucial in tolerance to waterlogging. These physiological patterns are usable at the seedling stage to assess their waterlogging tolerance.
