High silicon concentrations in grasses are linked to environmental conditions and not associated with C4 photosynthesis

Abstract

The uptake and deposition of silicon (Si) as silica phytoliths is common among land plants and is associated with a variety of functions. Among these, herbivore defense has received significant attention, particularly with regard to grasses and grasslands. Grasses are well known for their high silica content, a trait which has important implications ranging from defense to global Si cycling. Here, we test the classic hypothesis that C₄ grasses evolved stronger mechanical defenses than C₃ grasses through increased phytolith deposition, in response to extensive ungulate herbivory ("C₄ -grazer hypothesis"). Despite mixed support, this hypothesis has received broad attention, even outside the realm of plant biology. Because C₃ and C₄ grasses typically dominate in different climates, with the latter more abundant in hot, dry regions, we also investigated the effects of water availability and temperature on Si deposition. We compiled a large dataset of grasses grown under controlled environmental conditions. Using phylogenetically informed generalized linear mixed models and character evolution models, we evaluated whether photosynthetic pathway or growth condition influenced Si concentration. We found that C₄ grasses did not show consistently elevated Si concentrations compared with C₃ grasses. High temperature treatments were associated with increased concentration, especially in taxa adapted to warm regions. Although the effect was less pronounced, reduced water treatment also promoted silica deposition, with slightly stronger response in dry habitat species. The evidence presented here rejects the "C₄ -grazer hypothesis." Instead, we propose that the tendency for C₄ grasses to outcompete C₃ species under hot, dry conditions explains previous observations supporting this hypothesis. These findings also suggest a mechanism via which anthropogenic climate change may influence silica deposition in grasses and, by extension, alter the important ecological and geochemical processes it affects.

Keywords: C4 photosynthesis; grass; grassland; herbivore; phytolith; silicon.