How and Why Do Species Break a Developmental Trade-off? Elucidating the Association of Trichomes and Stomata Across Species

Premise: Previous studies have suggested a trade-off between trichome density (D) and stomatal density (D) due to shared cell precursors. We clarified how, when, and why this developmental trade-off may be overcome across species.

Methods: We derived equations to determine the developmental basis for D and D in trichome and stomatal indices (i and i) and the sizes of epidermal pavement cells (e), trichome bases (t), and stomata (s) and quantified the importance of these determinants of D and D for 78 California species. We compiled 17 previous studies of D-D relationships to determine the commonness of D-D associations. We modeled the consequences of different D-D associations for plant carbon balance.

Results: Our analyses showed that higher D was determined by higher i and lower e, and higher D by higher i and lower e. Across California species, positive D-D coordination arose due to i-i coordination and impacts of the variation in e. A D-D trade-off was found in only 30% of studies. Heuristic modeling showed that species sets would have the highest carbon balance with a positive or negative relationship or decoupling of D and D, depending on environmental conditions.

Conclusions: Shared precursor cells of trichomes and stomata do not limit higher numbers of both cell types or drive a general D-D trade-off across species. This developmental flexibility across diverse species enables different D-D associations according to environmental pressures. Developmental trait analysis can clarify how contrasting trait associations would arise within and across species.