Symplastic Phloem Loading in Poplar

Abstract

Sap is driven through phloem sieve tubes by an osmotically generated pressure gradient between source and sink tissues. In many plants, source pressure results from thermodynamically active loading in which energy is used to transfer sucrose (Suc) from mesophyll cells to the phloem of leaf minor veins against a concentration gradient. However, in some species, almost all trees, correlative evidence suggests that sugar migrates passively through plasmodesmata from mesophyll cells into the sieve elements. The possibility of alternate loading mechanisms has important ramifications for the regulation of phloem transport and source-sink interactions. Here, we provide experimental evidence that, in gray poplar (Populus tremula 3 Populus alba), Suc enters the phloem through plasmodesmata. Transgenic plants were generated with yeast invertase in the cell walls to prevent Suc loading by this route. The constructs were driven either by the constitutive 35S promoter or the minor vein-specific galactinol synthase promoter. Transgenic plants grew at the same rate as the wild type without symptoms of loading inhibition, such as accumulation of carbohydrates or leaf chlorosis. Rates of photosynthesis were normal. In contrast, alfalfa (Medicago sativa) plants, which have limited numbers of plasmodesmata between mesophyll and phloem, displayed typical symptoms of loading inhibition when transformed with the same DNA constructs. The results are consistent with passive loading of Suc through plasmodesmata in poplar. We also noted defense-related symptoms in leaves of transgenic poplar when the plants were abruptly exposed to excessively high temperatures, adding to evidence that hexose is involved in triggering the hypersensitive response.

Sap flow and sugar transport in plants

“…At the same time, the global sugar concentration in the leaves was higher than in herbaceous plants Davidson, Keller, and Turgeon, 2011;Fu et al, 2011). They had an open vein configuration and were accordingly called passive symplasmic loaders (Turgeon and Medville, 1998) and they appear to be in good agreement with Münch's original idea (Münch, 1930) that sucrose synthesized in the mesophyll moves down its concentration gradient to the minor veins, where it easily can enter the companion cells through the abundant plasmodesmata at the bundle sheath-companion cell interface (Zhang et al, 2014);see Fig. 12.…”

Dynamic and diverse sugar signaling

“…Plant sugar responses are also significantly influenced by phosphate levels [33]. Although sucrose is the main sugar for systemic transport from source to sink in plants [38], many of the sugar responses observed in plants are channeled through invertases or sucrose synthases [7,39] to generate glucose and other signaling sugars to trigger signal transduction via direct perception by diverse sensors or indirect signaling by energy and metabolite sensors. However, compelling evidence also supports multiple sucrose signaling pathways (Figure 1) [3,5].…”

“…Manipulations of key enzymes involved in sugar and starch metabolism have started to provide new insights into how the physiological sugar levels modulated by light, CO 2 and photoperiod alter gene expression and plant developmental processes [7, 9,36,38,45, 60,61,63*, 80–85]. Many key questions remain to be answered regarding the signaling actions of physiological levels of sugar signals in extracellular spaces and in different subcellular compartments [7,38].…”

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

“…Poplar is a so-called passive symplasmic loader, a type mostly found in tree species (Davidson et al, 2011). 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).…”