Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus

Abstract

A recurring theme in morphogenesis is the coupling of the expression of genes that drive morphogenesis and the morphogenetic process per se. This coupling ensures that gene expression and morphogenesis are carried out in synchrony. Morphogenesis of the spore-filled fruiting bodies in Myxococcus xanthus illustrates this coupling in the construction of a multicellular structure. Fruiting body formation involves two stages: aggregation of cells into mounds and the position-specific sporulation of cells that have accumulated inside mounds. Developmental gene expression propels these two processes. In addition, gene expression in individual cells is adjusted according to their spatial position. Progress in the understanding of the cell surface-associated C-signal is beginning to reveal the framework of an intercellular signalling system that allows the coupling of gene expression and multicellular morphogenesis. Accumulation of the C-signal is tightly regulated and involves transcriptional activation of the csgA gene and proteolysis of the full-length CsgA protein to produce the shorter cell surface-associated 17 kDa C-signal protein. The C-signal induces aggregation, sporulation and developmental gene expression at specific thresholds. The ordered increase in C-signalling levels, in combination with the specific thresholds, allows the C-signal to induce these three processes in the correct temporal order. The contact-dependent C-signal transmission mechanism, in turn, guarantees that C-signalling levels reflect the spatial position of individual cells relative to other cells and, thus, allows the cells to decode their spatial position during morphogenesis. By this mechanism, individual cells can tailor their gene expression profile to one that matches their spatial position. In this scheme, the molecular device that keeps gene expression in individual cells in register with morphogenesis is the C-signalling system, and the morphological structure, which is assessed, is the spatial position of individual cells relative to that of other cells.