Plant Osmoregulation as an Emergent Water-Saving Adaptation

Soil salinity affects plant transpiration and growth through two main pathways: the osmotic effect of salt in the soil (osmotic stress; analogous to water stress) and the toxic effect of salt within the plant (ionic stress; salt specific). However, the drastic and sudden reduction of transpiration exhibited by most species in response to an increase of salinity in the root zone is mainly associated with the osmotic phase, while ionic stress appears at a later time, causing the premature senescence of leaves and the reduction of the plant photosynthetic area. To better investigate the effects of salinity on plant-water relations, we introduce a parsimonious soil-plant-atmosphere continuum (SPAC) model accounting for both salt exclusion at the root level and osmoregulation-i.e.,the adjustment of internal water potential in response to salt stress. The model is used to interpret a paradox observed in salt-tolerant species where transpiration is maximum at an intermediate value of salinity (C-Tr,C-max), and is lower in more fresh (C < C-Tr,C-max) and more saline (C > C-Tr,C-max) conditions. Such nonmonotonic transpiration-salt concentration (T-r-C) patterns can be largely explained by plant osmoregulation, while the peak of transpiration at C-Tr,C- max tends to disappear over longer time scales, when ionic stress appears and morphological adaptations become predominant. Osmoregulation emerges here as a water-saving behavior similar to the strategies that xerophytes use to cope with aridity. The maximum of transpiration at C-Tr,C- max is thus the result of a trade-off between the enhancement of salt-tolerance and optimal carbon assimilation. Plain Language Summary Soil salinization represents a major threat for the food security and sustainable development of drylands, with salt affected soils-presently covering more than 9 billion ha worldwide-expected to further increase due to climate change, land use modifications and erroneous irrigation/groundwater abstraction practices. Despite this fact, the effects of salinity on the rate at which plants transpire and grow in salt affected soils are rarely considered in ecological and ecohydrological models, and the different processes leading to salt tolerance are yet poorly understood. Here, we introduce a simple model of how salt tolerant species adapt to elevated salt concentrations in the soil, and of how such adaptations substantially lead to plant osmoregulation, as an emergent water-saving behavior similar to the strategies that aridity-tolerant species (xerophytes) use to cope with extreme water scarcity. The bottom line is that salt-tolerant plants experience salt-stress as an alternative form of water-limitation, and developed both short-and long-term adaptations accordingly. Our findings are instrumental to a better comprehension of the interplay between soil salinization, salt tolerance and efficient water use that is, in turn, the key to understand the potential of salt-tolerant crops and contrast soil salinization.