The uncharacterized gene EVE contributes to vessel element dimensions in Populus

Significance Flowering plants exhibit exceptional diversity of form and stature. Their ability to achieve great heights is supported in part by their water-conducting specialized cells, the vessel elements, which have gradually evolved and resulted in increased hydraulic efficiency. Here we report the discovery, functional, and evolutionary analysis of a previously uncharacterized gene, ENLARGED VESSEL ELEMENT (EVE), that contributes to vessel element dimensions in the perennial woody species Populus. EVE’s appearance among the streptophyte algae and ultimate expansion in flowering plants may represent an important addition to the genetic toolkit required for plant vascular development. Surprisingly, EVE homologs are also detected in algae-infecting prasinoviruses, suggesting that it has been horizontally transferred.
The radiation of angiosperms led to the emergence of the vast majority of today’s plant species and all our major food crops. Their extraordinary diversification occurred in conjunction with the evolution of a more efficient vascular system for the transport of water, composed of vessel elements. The physical dimensions of these water-conducting specialized cells have played a critical role in angiosperm evolution; they determine resistance to water flow, influence photosynthesis rate, and contribute to plant stature. However, the genetic factors that determine their dimensions are unclear. Here we show that a previously uncharacterized gene, ENLARGED VESSEL ELEMENT (EVE), contributes to the dimensions of vessel elements in Populus, impacting hydraulic conductivity. Our data suggest that EVE is localized in the plasma membrane and is involved in potassium uptake of differentiating xylem cells during vessel development. In plants, EVE first emerged in streptophyte algae, but expanded dramatically among vessel-containing angiosperms. The phylogeny, structure and composition of EVE indicates that it may have been involved in an ancient horizontal gene-transfer event.