Stomatal density and mechanics are critical for high productivity: insights from amphibious ferns.

Angiosperm dominance in terrestrial landscapes is partially attributable to high photosynthetic capacities. Angiosperms benefit from diverse anatomical and physiological adaptations, making it difficult to determine which factors may have been prerequisites for the evolution of enhanced photosynthetic rates in this group. We employed a novel approach to this problem: comparisons between angiosperms and Marsileaceae, a family of semi-aquatic ferns that are among the only land plants to match angiosperm photosynthetic rates. We found that Marsileaceae have very high stomatal densities and, like angiosperms but unlike all other ferns previously studied, exhibit wrong-way stomatal responses to excision. These results suggest that stomatal density and a little-studied angiosperm trait, the capacity for lateral displacement of guard cells into neighboring epidermal cells, are crucial for facilitating high rates of gas exchange. Our analysis also associates these adaptations in Marsileaceae with an increased risk of excessive water loss during drought. Our findings indicate that evolution in stomatal physiology was a prerequisite for high photosynthetic capacities in vascular plants and a key driver of the abrupt Cretaceous rise of the angiosperms.