Intersection of transfer cells with phloem biology—broad evolutionary trends, function, and induction

Abstract

Transfer cells (TCs) are ubiquitous throughout the plant kingdom. Their unique ingrowth wall labyrinths, supporting a plasma membrane enriched in transporter proteins, provides these cells with an enhanced membrane transport capacity for resources. In certain plant species, TCs have been shown to function to facilitate phloem loading and/or unloading at cellular sites of intense resource exchange between symplasmic/apoplasmic compartments. Within the phloem, the key cellular locations of TCs are leaf minor veins of collection phloem and stem nodes of transport phloem. In these locations, companion and phloem parenchyma cells trans-differentiate to a TC morphology consistent with facilitating loading and re-distribution of resources, respectively. At a species level, occurrence of TCs is significantly higher in transport than in collection phloem. TCs are absent from release phloem, but occur within post-sieve element unloading pathways and particularly at interfaces between generations of developing Angiosperm seeds. Experimental accessibility of seed TCs has provided opportunities to investigate their inductive signaling, regulation of ingrowth wall formation and membrane transport function. This review uses this information base to explore current knowledge of phloem transport function and inductive signaling for phloem-associated TCs. The functional role of collection phloem and seed TCs is supported by definitive evidence, but no such information is available for stem node TCs that present an almost intractable experimental challenge. There is an emerging understanding of inductive signals and signaling pathways responsible for initiating trans-differentiation to a TC morphology in developing seeds. However, scant information is available to comment on a potential role for inductive signals (auxin, ethylene and reactive oxygen species) that induce seed TCs, in regulating induction of phloem-associated TCs. Biotic phloem invaders have been used as a model to speculate on involvement of these signals.

Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency

“…2, C-E). Tissues within this region are known to be responsible for solute transfer into the grain (Fisher and Cash-Clark, 2000;Andriunas et al, 2013) and are structurally arranged to facilitate the flow and release of solute into the endosperm Radchuk and Borisjuk, 2014). The implication is that individual grains responded to illumination by increasing the influx of water/solutes, evident by local changes of tissue parameters along the main transport route.…”

OPT3 Is a Phloem-Specific Iron Transporter That Is Essential for Systemic Iron Signaling and Redistribution of Iron and Cadmium inArabidopsis

“…Iron was also associated with minor veins of leaves of the opt3-3 mutant stained with Perls' stain (Supplemental Figure 7). Because minor veins and the leaf periphery are the sites of the preferential expression of OPT3 ( Figure 6B) and are the sites of the intensive xylem-to-phloem transfer (Bouche-Pillon et al, 1994;Turgeon and Webb 1973;Andriunas et al, 2013), we propose that OPT3 loads Fe into the phloem by mediating xylem-to-phloem cycling.…”

“…The tissue-and cell-type specificity of OPT3 expression, along with results from subcellular localization and uptake studies (Figures 1, 3, and 5) suggest that OPT3 may function in OPT3 Loads Fe into the Phloemapoplastic loading of transition ions into the phloem companion cells/sieve element complex (CC/SE) for subsequent long-distance transport. In addition, because xylem-to-phloem transfer is suggested to occur at the nodal regions in the stem as well as in minor veins in leaves (Bouche-Pillon et al, 1994;Andriunas et al, 2013), which are the sites of the preferential expression of OPT3 ( Figures 6B and 6C), we hypothesized that OPT3 participates in xylem-tophloem transfer of transition elements.…”

“…In addition to symplastic and apoplastic loading of the CC/CE complex, efficient xylem-to-phloem transfer may occur along the long-distance transport pathway with hubs at the nodal regions in the stem and minor veins in the leaf blade (Bouche-Pillon et al, 1994;Andriunas et al, 2013). The companion cells in these places differentiate into transfer cells to enhance membrane transport capacity and phloem loading and redistribution of resources (Andriunas et al, 2013). We found that (1) OPT3 is expressed in the phloem of minor veins in leaves and at the nodal sections of the stem (Figure 6), where it is associated with companion cells (Mustroph et al, 2009).…”

Papel de COPT1, COPT2, MTP2 y ZIP6 en el transporte y la homeostasis de metales en Medicago truncatula

“…En los nodos del tallo y ramificaciones del cilindro vascular, los nutrientes minerales pueden ser transferidos directamente desde el xilema al floema (Andriunas et al, 2013). Una gran parte del contenido mineral de la semilla proviene de la remobilización de nutrientes desde hojas ya senescentes (Himelblau & Amasino, 2001).…”