Autocrine Peptides, Self-organization and Zombie Cells: Molecular Switches in Phloem Formation

The evolution of the plant vascular system has had a crucial impact on the biosphere and earth history, because it enabled plants to effectively colonize land. Plant vasculature comprises two distinct transport systems, xylem and phloem. Xylem consists of connected vessels, which transport water and nutrients extracted from the soil to the rest of the plant body. Phloem is a more complex and versatile tissue, which distributes photosynthetic sugars, nutrients as well as developmental signals throughout the plant, typically from source to sink organs. Phloem sap conduits are formed by connected sieve elements, whose differentiation includes cell elongation, wall thickening and enucleation. Little is known about the molecular-genetic control of this vital differentiation process. The growth apices of plants, the meristems, connect to established vasculature via continuous production of early phloem, so-called protophloem. An ideal system to investigate this process is the Arabidopsis root meristem, where protophloem strand formation can be followed along the spatio-temporal gradient of single cell files. Over the last years, we have defined a molecular-genetic network that consists of two antagonistic modules and guides the formation of root protophloem sieve elements, starting from their stem cells. The positive regulators include polar plasma membrane-associated proteins that localize opposite to each other, while the negative regulators comprise receptor-like kinase signalling pathways that convey the response to autocrine peptide ligands. Because all positive and negative regulators identified so far are expressed from the beginning to the end of the differentiation process, developing protophloem cells must eventually escape their autocrine peptide signals to switch from proliferation to differentiation in a self-organizing spatio-temporal manner.