Avoiding transport bottlenecks in an expanding root system: Xylem vessel development in fibrous and pioneer roots under field conditions

Abstract

Root systems develop to effectively absorb water and nutrients and to rapidly transport these materials to the transpiring shoot. In woody plants, roots can be born with different functions: fibrous roots are primarily used for water and nutrient absorption, whereas pioneer roots have a greater role in transport. Because pioneer roots extend rapidly in the soil and typically quickly produce fibrous roots, they need to develop transport capacity rapidly so as to avoid becoming a bottleneck to the absorbed water of the developing fibrous roots and, as we hypothesized, immediately activate a specific type of autophagy at a precise time of their development. Using microscopy techniques, we monitored xylem development in Populus trichocarpa roots in the first 7 d after emergence under field conditions. Newly formed pioneer roots contained more primary xylem poles and had larger diameter tracheary elements than fibrous roots. While xylogenesis started later in pioneer roots than in fibrous, it was completed at the same time, resulting in functional vessels on the third to fourth day following root emergence. Programmed cell death was responsible for creating the water conducting capacity of xylem. Although the early xylogenesis processes were similar in fibrous and pioneer roots, secondary vascular development proceeded much more rapidly in pioneer roots. Compared to fibrous roots, rapid development of transport capacity in pioneer roots is not primarily caused by accelerated xylogenesis but by larger and more numerous tracheary elements and by rapid initiation of secondary growth.