Anatomical adaptations in aquatic and wetland dicot plants: Disentangling the environmental, morphological and evolutionary signals

Understanding how plants adjust their internal structures to withstand adverse environmental conditions is vital for predicting their responses to ongoing environmental change. Plants have repeatedly evolved small water transporting conduits and large storage parenchyma tissues to cope with anoxia, freezing- or drought-induced damages. However, how these adaptations evolved in unrelated taxa across hydrological and thermal gradients, remains unclear. Here we show that stem anatomical variations in 212 European aquatic and wetland dicots are driven by thermal and hydrological constraints via control over plant size, growth form, and leaf traits, while phylogenetic constraints have only a weak effect. Phylogenetic comparative analyses controlling for confounding factors showed that both waterlogging (anoxia) and low-temperature promote smaller plants with reduced vessel conduits and limited lignification, but extended parenchyma and hence storage and tissue renewal capacity to secure resilience to biomass loss induced by running water or frost disturbances. Decreasing water depth and anoxia promote larger wetland plants with thick-walled libriform fibers, large vessels with simple perforation plates securing high hydraulic efficiency, and semi-ring porous xylem with wide earlywood vessels in spring and narrow latewood vessels in summer, providing both efficiency and safety in water transport. The aquatic environment promotes plants with a large cortex zone with photosynthetic chlorenchyma and starch-storing parenchyma cells along with extensive air spaces that provide aeration and buoyancy. Low temperatures promote short-stature forbs with smaller vessels, scalariform perforation plate, extended parenchyma, resulting in reduced embolism risk. Although most anatomical variation was explained by differences between aquatic and wet terrestrial growth forms, environmental gradients, plant size, and leaf properties exerted a significant control on plant tissue structures not confounded by phylogenetic inertia. Distinct habitats, spread across broad thermal and hydrological gradients, harbor unrelated species with different evolutionary histories that have converged to similar anatomical and hence morphological structures.

Automated summary

Research indicates that plants adjust their internal structures to withstand adverse conditions and evolve similar morphological structures under thermal and hydrological gradients.