Evolution of arborescence at hydraulic, structural, and developmental limits

The repeated, parallel evolution of tree-like plants raises the question of how different lineages, extant and extinct, addressed the shared hydraulic and mechanical challenges of increasing stature through diverse developmental means. A previously overlooked challenge of increased size is the increasing likelihood of mortality under drought due to the spread of gas-phase blockage (embolism) throughout any expanding water conduit networks if they are highly integrated. Here, we draw on the known diversity of tree-like plants among living and extinct lineages to reframe arborescence as the open-ended (developmentally indeterminate) growth and survival of a central trunk. We first contrast the developmental models for tall plant growth of canonical seed plant trees (featuring a crown of woody branches borne by a tall woody stem), palms, and tree ferns, not all of which have trunks capable of indeterminate growth. We consider the early evolution of wood anatomy in the context of a striking convergence among tall plants towards sparsely connected vascular networks. We then propose that vascular disconnection may be a key adaptation allowing for the persistence of a single central trunk and a major factor driving the early evolution of wood anatomy. We next survey the vascular diversity of tall plants to query more generally the developmental and functional prerequisites of open-ended trunk growth. Finally, we consider what perspectives and research opportunities are provided by this framing of the evolution of arborescence and what challenges take on a new urgency.