Source-to-sink transport of sugar and regulation by environmental factors

Abstract

Source-to-sink transport of sugar is one of the major determinants of plant growth and relies on the efficient and controlled distribution of sucrose (and some other sugars such as raffinose and polyols) across plant organs through the phloem. However, sugar transport through the phloem can be affected by many environmental factors that alter source/sink relationships. In this paper, we summarize current knowledge about the phloem transport mechanisms and review the effects of several abiotic (water and salt stress, mineral deficiency, CO2, light, temperature, air, and soil pollutants) and biotic (mutualistic and pathogenic microbes, viruses, aphids, and parasitic plants) factors. Concerning abiotic constraints, alteration of the distribution of sugar among sinks is often reported, with some sinks as roots favored in case of mineral deficiency. Many of these constraints impair the transport function of the phloem but the exact mechanisms are far from being completely known. Phloem integrity can be disrupted (e.g., by callose deposition) and under certain conditions, phloem transport is affected, earlier than photosynthesis. Photosynthesis inhibition could result from the increase in sugar concentration due to phloem transport decrease. Biotic interactions (aphids, fungi, viruses…) also affect crop plant productivity. Recent breakthroughs have identified some of the sugar transporters involved in these interactions on the host and pathogen sides. The different data are discussed in relation to the phloem transport pathways. When possible, the link with current knowledge on the pathways at the molecular level will be highlighted.

Keywords: Phloem; abiotic factors; biotic factors; source/sink; sugar transport.

FIGURE 1

Comparison of source-to-sink sugar transport in symplastic and apoplastic active phloem loaders. Sucrose available for export from mesophyll cells (MC) results from a balance between storage in the vacuoles and sequestration as starch in the chloroplasts. Sucrose can reach the sieve tubes through plasmodesmata that allow for its diffusion from cell to cell in species like cucurbits. Sucrose is converted to larger molecules (RFOs) by the sequential addition of galactosyl residues in modified companion cells (CC) called intermediary cells. The larger molecules cannot move back to phloem parenchyma cells (PP) and are transferred and accumulated in sieve tubes. In apoplast-loading species, sucrose reaches phloem parenchyma cells through plasmodesmata. Sucrose is loaded and accumulates in the phloem by passing through the apoplast between the PP and the CC. The major players are presented in the enlargement of that area. Sucrose enters the apoplast through facilitators of the SWEET family (pale green circle) and is accumulated in the companion cell by a proton/sucrose co-transporter of the SUT1/SUC2 type (green circle). The energy necessary for the co-transport is provided by an H+/pumping ATPase (black circle) which establishes a proton gradient and a trans-membrane potential regulated by potassium channels of the AKT2/3 type (white circle). In Solanaceous species, SUT1 transporters are localized at the plasma membrane of sieve elements (not shown). Polyols can also be transported into the phloem, with specific transporters located in the plasma membrane of CC (not shown). A high hydrostatic pressure is generated in the sieve tubes of the collection phloem and water from the xylem is attracted. Sucrose, RFOs and polyols are transported in the sieve tubes to the sink organs in the transport phloem. All along the path, they can be leaked from and reloaded into the phloem via the same mechanism (not shown). Sucrose is unloaded into the release phloem where the hydrostatic pressure is supposed to be lower. Sucrose can be unloaded through a symplastic pathway or through an apoplastic pathway. In the latter case, sucrose is unloaded into the apoplast through specific carriers which can be of the SUT1/SUC2 type (green circle; Carpaneto et al., 2005). Sucrose is then taken up by sink-specific sucrose carriers of the same SUT1/SUC2 (light green circle) or converted to hexoses by a cell-wall invertase (CWInv). Hexoses are then taken up by specific carriers at the plasma membrane (orange circle) or at the tonoplast level (yellow and brown circles). Sucrose in sink cells can be metabolized (growing sinks) or stored as starch in amyloplasts, or imported into the vacuoles (red circles) and further converted to hexoses by a vacuolar invertase (VInv).

FIGURE 2

Model of the plant’s responses to mineral nutrient deficiency. (A) Response to nitrate and phosphorus deficiency: deficiency in nitrogen and phosphorus leads to reduced photosynthesis, accumulation of sugars in source leaves, increased carbon allocation to the roots and a higher root/shoot ratio. Moreover, phosphorus limitation induces an adaptation of the root system architecture: root hairs initiate and elongate, which increases the root surface area. AtSUC2 (green circle) is a component of the sugar-signaling pathway in the response to phosphorus starvation. (B) Response to magnesium and potassium deficiency: Mg deficiency increases the concentration of soluble sugars and starch in leaves and reduces leaf growth. Mg deficiency impacts sugar metabolism, as well as sucrose export to the roots. Mg deficiency reduces the Mg-ATP availability and the activity of H⁺-ATPase, thus reducing the driving force for sucrose phloem loading. AKT2/3 potassium channels affect sugar loading and long-distance transport by regulating the H^+/sucrose transporter. Conversely, K⁺-limitation rarely results in starch accumulation. MC, mesophyll cell; CC, companion cell; PP, parenchyma phloem; MC, mesophyll cell.

FIGURE 3

Simplified representation of the key players involved in the competition for sugars at the plant/microbe interface. Depending on the pathosystem, plants and microbes present efficient machineries to take up or modify apoplastic sucrose. In biotrophic interactions, sucrose can be taken up by both host and fungus via sucrose transporters, e.g., maize ZmSUT1 and fungus Ustilago maydis UmSRT1, respectively. However, glucose is the main carbon source transferred from the host to the parasite and is essential for the feeding and metabolism of the parasite. Cell wall invertases from host and microbes contribute to the source of hexoses at the apoplast level. Hexose transporters allow pathogenic or mutualistic fungi to preferentially compete for glucose and/or fructose (i.e., UfHXT1, BcFRT1, CgHXTs, GiMST2). To gain access to apoplastic hexoses, plants possess a large repertoire of STPs that can support host demand. Multiple roles of hexoses in host cells have been described; among others, hexoses can be used as an energy source or as signaling molecules and regulators of pathogenesis-related, photosynthetic and sink gene expression. An indirect consequence of host sucrose and hexose acquisition is a possible starvation of microbes through a limited access to sugar at the interface. Host sugar uptake can be bypassed in some pathogenic interactions. Specific effectors (not represented in the diagram) released by some bacteria and probably fungi can manipulate host sugar effluxers (SWEETs) and further make sucrose and hexoses available for the pathogen