How and why do species break a developmental trade-off? Elucidating the association of trichomes and stomata across species

Abstract

Premise

Previous studies have suggested a trade-off between trichome density (D_t) and stomatal density (D_s) 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_t and D_s in trichome and stomatal indices (i_t and i_s) and the sizes of epidermal pavement cells (e), trichome bases (t), and stomata (s) and quantified the importance of these determinants of D_t and D_s for 78 California species. We compiled 17 previous studies of D_t–D_s relationships to determine the commonness of D_t–D_s associations. We modeled the consequences of different D_t–D_s associations for plant carbon balance.

Results

Our analyses showed that higher D_t was determined by higher i_t and lower e, and higher D_s by higher i_s and lower e. Across California species, positive D_t–D_s coordination arose due to i_t–i_s coordination and impacts of the variation in e. A D_t–D_s 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_t and D_s, 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_t–D_s trade-off across species. This developmental flexibility across diverse species enables different D_t–D_s associations according to environmental pressures. Developmental trait analysis can clarify how contrasting trait associations would arise within and across species.