Evolution of water transport and xylem structure

Land plants need water to replace the evaporation that occurs while atmospheric CO2 is diffusing into photosynthetic tissue. The water-for-carbon exchange rate is poor, and evolutionary history indicates a progression of innovations for cheap water transport--beginning in order with capillary suction at cell walls, stomatal regulation, hydroids, tracheids, secondary xylem, endodermis, and vessels. The radiation of plants in the Silurian and Devonian occurred when the need for water was at an all-time low because of high CO2 concentration. Transport improvements appeared as water demand increased and CO2 dropped to current values in the Carboniferous and Permian. Stomatal regulation and high-conductivity conduits permitted larger plants and a transition from poikilohydric to homoiohydric water relations. The evolution of conduits from hydroids through tracheids to vessels reflects the need to balance resistance to implosion and cavitation versus maximum hydraulic conductance and minimum conduit investment. Localization of rigidifying lignin away from the lumen surface and porous wall regions during tracheid evolution, and the origin of pits, acted to maintain wall strength and permeability while minimizing cavitation. Vessels mark the pinnacle of efficiency, making vines and dense, stiff woods possible without sacrificing conductivity or cavitation resistance. However, vessels make cavitation-resistant wood more expensive and may compromise refilling efficiency versus tracheids. Vascular networks maximize hydraulic conductivity and protection from cavitation at minimum investment by following Murray's law and localizing resistances to the periphery. A future challenge is to quantify the significance of xylem structure in terms of the carbon cost of transpiration and the net carbon profit via gas exchange.