Vessel development and the importance of lateral flow in water transport within developing bundles of current-year shoots of grapevine (Vitis vinifera L.)

Abstract

In the developing xylem bundles of young stems, the presence of immature living vessel elements can strongly restrict or even block axial hydraulic conductance, especially in newly matured vessels. Lateral connections between vessels may provide an alternative pathway for water movement to bypass these closed, living elements. Using the grapevine as a model system, the present study aimed to demonstrate the effects of living vessel elements on water movement patterns, and the importance of lateral flow for effective water conductivity in the developing bundles. Living vessel elements were detected using dye staining and the pattern of vessel development and maturation was then monitored. The importance of lateral flow was confirmed using several approaches: (1) capacity for lateral flow, (2) effect of increasing the distance of water transport, and (3) effect of ion concentrations. Living vessel elements were found along the developing bundles, they occupied a significant proportion of the distal and peripheral parts of the flow path, forming a substantial barrier to apoplastic water flow. Water in the developing xylem bundles could move easily from vessel to vessel and between secondary and primary xylem. Furthermore, data from increasing the transport length and altering the ion concentrations supported the critical contribution of the lateral flow to the total hydraulic conductance within the developing bundles. The hydraulic architecture of the developing xylem bundles is described. The results are discussed in terms of reliability and efficiency of water transport during shoot growth and development.

Grapevine Xylem Development, Architecture, and Function

“…Within a single vessel, individual vessel elements die at different times, although usually starting first basally and progressing in the apical direction. Both open basal and closed apical vessel elements may be found simultaneously within a single vessel (Esau 1936;Eames and MacDaniels 1947;Halis et al 2012). Thus, individual vessel elements may become hydraulically active before the entire vessel activates (Halis et al 2012) and the end walls of still living vessels form the barrier between the apoplast and symplast during this time.…”

“…Both open basal and closed apical vessel elements may be found simultaneously within a single vessel (Esau 1936;Eames and MacDaniels 1947;Halis et al 2012). Thus, individual vessel elements may become hydraulically active before the entire vessel activates (Halis et al 2012) and the end walls of still living vessels form the barrier between the apoplast and symplast during this time. Once all of the vessel elements within a vessel undergo autolysis, the vessel becomes fully hydraulically functional, with water able to move from element to element through open perforation plates along the entire length of a vessel or through pits into lateral vessels.…”

“…Other cellular changes also occur, including the rupture of the tonoplast, the degradation of other organelles within the cell, and the deposition of lignin (reviewed in Fukuda 1997 andBollhöner et al 2012). At this stage, each individual vessel element maintains end walls and intact cell membranes filled with dilute protoplasm and may remain in this stage for up to several weeks (Esau and Hewitt 1940;Halis et al 2012;Bollhöner et al 2012).…”

Impact of Electroviscosity on the Hydraulic Conductance of the Bordered Pit Membrane: A Theoretical Investigation

“…1, C and D). Pits redistribute flux to bypass immature vessels in young shoots (Halis et al, 2011) and local emboli ( Fig. 1B; Tyree and Ewers, 1991) and function as valves between adjacent vessels, allowing the passage of sap while preventing the spread of embolisms (Konrad and RothNebelsick, 2005;Choat et al, 2008;Jansen et al, 2009) and pathogens (Roper et al, 2007).…”

Alterações anatômicas do sistema vascular em porta-enxertos de videira

“…Com estes resultados, salienta-se a importância de conexões entre os elementos de vaso, transporte lateral e vias alternativas para o transporte de água, uma vez que a estrutura do xilema apresenta-se diferentemente entre as zonas do ápice, mediana e base dos ramos. Conforme também apontado por Halis et al (2012), o fluxo lateral de água e as conexões entre os vasos representam papel essencial no fluxo de seiva.…”