Cell-Autonomous and Non-Cell-Autonomous Mechanisms Concomitantly Regulate the Early Developmental Pattern in the Kelp Saccharina latissima Embryo

Abstract

Brown algae are multicellular organisms that have evolved independently from plants and animals. Knowledge of the mechanisms involved in their embryogenesis is available only for the Fucus, Dictyota, and Ectocarpus, which are brown algae belonging to three different orders. Here, we address the control of cell growth and cell division orientation in the embryo of Saccharina latissima, a brown alga belonging to the order Laminariales, which grows as a stack of cells through transverse cell divisions until growth is initiated along the perpendicular axis. Using laser ablation, we show that apical and basal cells have different functions in the embryogenesis of this alga, with the apical cell being involved mainly in growth and basal cells controlling the orientation of cell division by inhibiting longitudinal cell division and thereby the widening of the embryo. These functions were observed in the very early development before the embryo reached the 8-cell stage. In addition, the growth of the apical and basal regions appears to be cell-autonomous, because there was no compensation for the loss of a significant part of the embryo upon laser ablation, resulting in smaller and less elongated embryos compared with intact embryos. In contrast, the orientation of cell division in the apical region of the embryo appears to be controlled by the basal cell only, which suggests a polarised, non-cell-autonomous mechanism. Altogether, our results shed light on the early mechanisms of growth rate and growth orientation at the onset of the embryogenesis of Saccharina, in which non-cell-specific cell-autonomous and cell-specific non-cell-autonomous processes are involved. This complex control differs from the mechanisms described in the other brown algal embryos, in which the establishment of embryo polarity depends on environmental cues.