The diversity of stomatal development regulation in Callitriche is related to the intrageneric diversity in lifestyles

Stomata, the gas exchange structures of plants, are formed by the division and differentiation of stem cells, or meristemoids. Although diverse patterns of meristemoid behavior have been observed among different lineages of land plants, the ecological significance and diversification processes of these different patterns are not well understood. Here we describe an intrageneric diversity in the patterns of meristemoid division within the ecologically diverse genus Callitriche (Plantaginaceae). Meristemoids underwent a series of divisions before differentiating into stomata in the terrestrial species of Callitriche, but these divisions did not occur in amphibious species, which can grow in both air and water, in which meristemoids differentiated directly into stomata. These findings imply the adaptive significance of diversity in meristemoid division. Molecular genetic analyses showed that the different expression times of the stomatal key transcription factors SPEECHLESS and MUTE, which maintain and terminate the meristemoid division, respectively, underlie the different division patterns of meristemoids. Unlike terrestrial species, amphibious species prematurely expressed MUTE immediately after expressing SPEECHLESS, which corresponded to their early termination of stomatal division. By linking morphological, ecological, and genetic elements of stomatal development, this study provides significant insight that should aid ecological evolutionary developmental biology investigations of stomata.

Automated summary

This study explores the intrageneric diversity in the patterns of meristemoid division within the ecologically diverse genus Callitriche. Terrestrial and amphibious species of Callitriche exhibit different division patterns of meristemoids before differentiating into stomata, which is associated with the expression times of the key transcription factors SPEECHLESS and MUTE. The findings imply the adaptive significance of diversity in meristemoid division and provide insights for ecological evolutionary developmental biology investigations of stomata.