Natural Variation in the Ability to Endure Inundation by Water

Strong variation exists in the ability to withstand conditions of low oxygen availability. Many terrestrial plant species, including nearly all crops, are sensitive and do not survive longer than a few days of waterlogging. At the other extreme are plants adapted to life in wetlands (swamps, marshes, bogs, etc.), such as Iris pseudacorus, Typha latifolia, Phragmites australis and Rorippa sylvestris.

They can tolerate submergence for months (Bailey-Serres et al. 2012b) and thus are adapted to primary hypoxia. Many other species show moderate tolerance of secondary hypoxia that reflects the hydrological signature of their natural environments—that is, variation in flooding tolerance determines, to a large extent, the distribution of plant species in the many areas worldwide that can be exposed to flooding. This can easily be seen in riparian vegetation, which shows pronounced zonation attributable to variation in flooding tolerance. A well-documented case is represented by the genus Rumex.

It comprises species that are more hypoxia tolerant (e.g. R. maritimus and R. palustris) and thrive in zones prone to extended flooding—for instance, in the Rhine Valley (Fig. 5.5, Table 5.2)—as well as more hypoxia-sensitive species (e.g. R. acetosa and R. acetosella), which are found in zones with less frequent and lower-amplitude flooding events. Similarly, certain tree species (e.g. of the genera Alnus, Populus, Salix and Quercus) dominate along rivers and in alluvial forests.

Fig. 5.5. Water level changes of the Rhine river near Nijmegen (the Netherlands) over 2 years, and vertical zonation of species differing in submergence tolerance. (Redrawn after Blom et al. (1993))

Table 5.2. Effect of flooding on biomass production and on nutrient content of the leaves of two flooding-sensitive representatives and one flooding-tolerant representative of the genus Rumex (After Laan et al. (1989))

In contrast to most cultivated plants, rice is flooding tolerant, and lowland rice varieties are normally grown in paddy fields (i.e. parcels of land covered with water 5-50 cm deep). Still, considerable intraspecific variation exists. Several low-yielding landraces are able to withstand particularly severe floods. Others can be directly planted as seeds into shallow paddies and develop despite low oxygen availability (Bailey-Serres and Voesenek 2008).

A wide range of mechanisms explains the distribution of plants in flood-prone environments. Some species (e.g. Chenopodium rubrum) are able to circumvent the adverse effects of hypoxia by completing their life cycle between floods—which in many habitats occur with certain regularity— and by enduring flooding events as dormant life stages (Blom and Voesenek 1996). Most other plants show morphological, anatomical, developmental and metabolic characteristics that help them to avoid or truly tolerate oxygen deprivation (Voesenek and Bailey-Serres 2015) (Fig. 5.6).

Fig. 5.6. Morphological and developmental adaptations or acclimative modifications that help flooding-tolerant plant species avoid anoxic conditions

Hypoxia survival traits represent a very good example of how plant stress endurance strategies have in recent years been elucidated from the organismic level to the molecular level, and from model plants to species initially studied purely ecophysiologically. This has been possible thanks to the fruitful collaboration of ecologists with molecular biologists. The current level of understanding has implications for agriculture too, as mechanistic insights can now be used in breeding programmes aimed at developing plant varieties better adapted to conditions that are becoming more prevalent because of climate change (Xu et al. 2006) (Box 5.1).