Sucrose transporters and plasmodesmal regulation in passive phloem loading

Abstract

An essential step for the distribution of carbon throughout the whole plant is the loading of sugars into the phloem in source organs. In many plants, accumulation of sugars in the sieve element-companion cell (SE-CC) complex is mediated and regulated by active processes. However, for poplar and many other tree species, a passive symplasmic mechanism of phloem loading has been proposed, characterized by symplasmic continuity along the pre-phloem pathway and the absence of active sugar accumulation in the SE-CC complex. A high overall leaf sugar concentration is thought to enable diffusion of sucrose into the phloem. In this review, we critically evaluate current evidence regarding the mechanism of passive symplasmic phloem loading, with a focus on the potential influence of active sugar transport and plasmodesmal regulation. The limited experimental data, combined with theoretical considerations, suggest that a concomitant operation of passive symplasmic and active phloem loading in the same minor vein is unlikely. However, active sugar transport could well play an important role in how passively loading plants might modulate the rate of sugar export from leaves. Insights into the operation of this mechanism has direct implications for our understanding of how these plants utilize assimilated carbon.

Regulation of Sucrose Transporters and Phloem Loading in Response to Environmental Cues

“…In poplar, down-regulation of the vacuolar Suc transporter PtaSUT4 via RNAi decreases source strength and leads to Suc accumulation in the leaf as well as lower photosynthetic activity (Payyavula et al, 2011;Frost et al, 2012). It can be hypothesized that PtaSUT4 activity regulates the cytosolic concentration of Suc in leaf mesophyll cells by controlling the exchange with the vacuole, thereby influencing the Suc gradient along the prephloem pathway that determines the rate of phloem loading (Liesche, 2017). This notion of PtaSUT4 as an important link between Suc production, storage, and export is confirmed here by showing that its expression scales with photosynthetic rate.…”

“…Plasmodesmata enable diffusion along the whole prephloem pathway from mesophyll cells to the SECCC, and the high Suc concentration in the source phloem is thought to be the result of high Suc levels in the cytosol of all leaf cells (Rennie and Turgeon, 2009;Zhang et al, 2014). However, the altered pattern of carbohydrate partitioning in plants that lack the tonoplast-localized PtaSUT4 indicates that active Suc transport could still be relevant for poplar phloem loading (Payyavula et al, 2011;Liesche, 2017). The question if Suc transporters are involved in the regulation of carbohydrate export from leaves in passive loaders is a special focus in this study.…”

Defoliation-induced compensatory transpiration is compromised inSUT4-RNAiPopulus

“…20 Sucrose compartmentalization involves its uptake into the vacuole by the tonoplast monosaccharide proton antiporter and its efflux into the cytosol by the tonoplast sucrose 22 proton symporter SUT4 (Reinders et al 2008;Schulz et al 2011;Schneider et al 2012). In Arabidopsis where phloem loading is active and mediated exclusively by plasma membrane 24 SUTs (Ayre 2011;Liesche 2017), AtSUT4 is very weakly expressed, representing less than 5% of leaf SUT transcript abundance (Lloyd and Zakhleniuk 2004;Schneider et al 2012). In the 26 monocot sorghum, the tonoplast SUT4 is as well expressed as plasma membrane SUTs in source leaves and thought to facilitate active phloem loading (Milne et al 2013).…”

Phloem structure and development in Illicium parviflorum, a basal angiosperm shrub

“…Despite the understory origins of woody angiosperms, organismal scaling of sieve tube elements of the phloem appears as a conserved mechanism that predates the origin of woody flowering plants, and likely seed plants in general (see Woodruff et al ., 2004; Liesche et al ., 2015; Liesche, 2017). Angiosperm colonization of the vertical niche implied a number of structural innovations that led to a higher functional efficiency and thus productivity (Koch et al ., 2004; Savage et al ., 2017; Gleason et al ., 2018).…”