Light intensity-regulated stomatal development in three generations of Lepidium sativum

Abstract

Stomata are of crucial importance for CO2 uptake and the water economy of terrestrial plants. They evolve during the early phases of leaf development according to genetically conserved information modulated in its expression by environmental conditions. Mature leaves experience the environment, e.g. light intensity, and signal to younger developing leaves, modifying stomatal density (SD) and probably other leaf traits as well. In addition, the parental environment can affect the offspring’s phenotypes in an adaptive manner. However, the transgenerational effect of light on SD and interactions with the offspring’s light environment have not been studied so far. Here we compare transgenerational (parental) and growth-light (environmental) effects on SD. We grew three generations of garden cress (Lepidium sativum) in two contrasting light environments in a full factorial design. Stomatal and pavement cell densities (SD, PCD), 13C abundance as a proxy of leaf internal CO2 concentration (Ci), and leaf area were analysed in cotyledons and first true leaves of parental plants and two generations of offspring. Our results indicate that SD of offspring reflects both current and maternal light intensities. The transgenerational effect of light on SD was much smaller than the influence of current growth light and the former’s manifestation was dependent on light experienced by offspring. The cotyledons’ SD was unresponsive to variations in Ci but retained its light sensitivity, though it was smaller than in true leaves. High light reduced amphistomy in favour of the lower (abaxial) leaf side. SD and PCD were linearly proportional irrespective of light level, indicating invariant portions of spacing and amplifying cell divisions, and causing lower sensitivity of stomatal index at high SD. We show that light-stimulated stomatal development in garden cress differs in cotyledons and true leaves, varies between adaxial and abaxial leaf sides, and retains transgenerational information about environmental clues.