Anatomical and Trait Analyses Reveal a Silicon-Carbon Trade-Off in the Epidermis of Sedges

In recent years, the detection of numerous negative correlations between silicon (Si) and carbon (C)-based compounds in plants has suggested trade-offs between different stress resistance and/or mechanical support strategies. However, nearly all studies have involved whole-leaf analysis, and it is unclear how the trade-off operates mechanistically, at the cellular level. Here we combined leaf trait measurements and microscopic analyses (electron microscopy with elemental X-ray mapping and X-ray microtomography) of 17 species from a high-Si family: Cyperaceae. Accumulation of Si was strongly negatively correlated with C-based compounds, particularly tannins. Our microscopical investigations showed that the accumulation of phenolics and deposition of silica were mutually exclusive in the outer epidermal cell walls. This trade-off was independent of that between the construction of tough, sclerenchyma-rich leaves and growth potential (the leaf economics spectrum). We also identified a strong negative correlation between Si and accumulation of epicuticular waxes. Previous whole leaf analyses were, in effect, hiding the locations of the trade-off between Si and C-based compounds in plants. The epidermal location of this trade-off and the specific involvement of tannins and waxes suggest the existence of different strategies to resist environmental stresses. Our study provides key insights into plant Si utilization and highlights the multidimensionality of plant stress resistance strategies.