Seed mucilage evolution: Diverse molecular mechanisms generate versatile ecological functions for particular environments

Plant myxodiasporous species have the ability to release a polysaccharidic mucilage upon imbibition of the seed (myxospermy) or the fruit (myxocarpy). This is a widespread capacity in angiosperms providing multiple ecological functions including higher germination efficiency under environmental stresses. It is unclear whether myxodiaspory has one or multiple evolutionary origins and why it was supposedly lost in several species. Here, we summarize recent advances on three main aspects of myxodiaspory. (a) It represents a combination of highly diverse traits at different levels of observation, ranging from the dual tissular origin of mucilage secretory cells to diverse mucilage polysaccharidic composition and ultrastructural organization. (b) An asymmetrical selection pressure is exerted on myxospermy-related genes that were first identified in Arabidopsis thaliana. The A. thaliana and the flax intra-species mucilage variants show that myxospermy is a fast-evolving trait due to high polymorphism in a few genes directly acting on mucilage establishment. In A. thaliana, these actors are downstream of a master regulatory complex and an original phylogenetic overview provided here illustrates that this complex has sequentially evolved after the common ancestor of seed plants and was fully established in the common ancestor of the rosid clade. (c) Newly identified myxodiaspory ecological functions indicate new perspectives such as soil microorganism control and plant establishment support.