When it is converted to sugar, that is in turn used by the plant for things like respiration, growth and reproduction. Some of the sugar is also stored for use later, by being converted into starch.
Plants make, and store temporary supplies of starch in their leaves, which they use during the night when there is no light available for photosynthesis. Many plants, including crop plants like wheat and potatoes, also make starch in their seeds and storage organs their grains and tubers , which is used for germination and sprouting.
But what exactly is starch? Starch is a chain of glucose molecules which are bound together, to form a bigger molecule, which is called a polysaccharide. There are two types of polysaccharide in starch:. As well as being important for plants, starch is also extremely important to humans. Starchy food for example is the main source of digestible carbohydrates in our diet. Sucrose can be unloaded through a symplastic pathway or through an apoplastic pathway.
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. These different pathways concern the loading of sucrose in the so-called collection phloem Van Bel, which represents the initial step of long-distance transport.
Transport along the path between source and sink occurs in the transport phloem and sucrose is delivered to sink organs by the release phloem Van Bel, At many stages along the pathway, specific transporters are involved in the cell-to-cell movement of sucrose or in the intracellular compartmentation between the cytoplasm and organelles; they thus represent major regulators of sugar fluxes.
It should be noted that sucrose transporters SUTs have been localized and characterized in the three phloem sections.
Sucrose can act as a signal and regulate many genes involved in growth and development Koch, ; Muller et al. During longitudinal transport, sucrose can be leaked and retrieved but also used by sink cells along the path axial sinks; Minchin and Thorpe, In some species, stems or petioles can be turned into storage organs e.
In such conditions, storage is transient as resources will later be used to support growth along with plant development. These organs successively act as sinks and sources Juchaux-Cachau et al. Concerning their ability to retrieve sucrose from the apoplast, the respective membrane potential levels between SEs and phloem parenchyma cells are decisive Hafke et al.
SUTs are involved in sucrose movement in the transport phloem, even in tree species where loading is symplastic in the collection phloem Turgeon, b. In the release phloem, sugars can exit the phloem through either a symplastic or an apoplastic pathway, although the first steps are often symplastic Fisher and Oparka, ; Patrick, However, unloading pathways depend on the particular sink involved and its development stage Figure 1.
In sinks like developing seeds or infected tissues, symplastic discontinuity requires an apoplastic step for the transfer of photo-assimilates. A switch from apoplastic to symplastic unloading was noted during potato tuberization Viola et al. In fruit development, contrasting results have been found: in grape berry, Zhang et al. In seeds, SUTs but also hexose transporters and cell-wall invertases are responsible for sugar movement but their respective roles differ depending on the development stage Weber et al.
These pathways have been extensively studied in legume seeds, together with the corresponding regulation of sucrose unloading Zhang et al. Sink organs depend on the delivery of sucrose or other forms of carbohydrates by the phloem for their growth and development. This creates a priority system among sinks. Roots and young leaves are major sinks during the early developmental stages, whereas tubers, fruit and seeds become major sinks during the reproductive stages Wardlaw, The distribution of resources among sinks is also a key factor of plant productivity based on the harvest index HI.
The HI is the ratio of harvested dry weight over plant dry weight or above-ground shoot dry weight : therefore a high HI indicates that a large amount of photo-assimilates has been diverted to the sinks harvested by humans Gifford et al.
In order for plants to reach a balanced development and optimize their reproductive fitness, priority for access to photo-assimilates needs to be established between sinks. Changes in carbon partitioning and switches between the apoplastic and symplastic pathways occur throughout development or as a response to the environment Roitsch, ; Godt and Roitsch, According to Wardlaw , the underlying basis of sink strength assuming a pressure flow mechanism for translocation is an ability to effectively lower the concentration of photo-assimilates in the SEs of the sinks and thus establish a favorable hydrostatic pressure gradient between the source and the sink.
In that respect, the role of cell-wall invertases has frequently been highlighted in sink organs as they increase sucrose unloading by converting sucrose to hexoses. Transport of photo-assimilates depends on source supply and sink demand.
The role of the phloem sap sugar content in the coupling between sink demand and source activity is still a matter of debate Minchin et al. However, high sucrose contents in leaves could have an inhibitory effect on SUT activity and thus inhibit sucrose loading into the phloem. This point was evidenced by feeding sucrose to the transpiration stream of cut sugar-beet leaves Chiou and Bush, The authors hypothesized that high sucrose concentrations in the vascular tissue, resulting from decreased sink demand, down-regulated transporter activity.
This could lead to decreased phloem loading and increased sugar levels in mesophyll cells, and in turn down-regulated photosynthesis. The opposite regulation is thought to occur in the case of increased sink demand Chiou and Bush, This link between sugar export in leaves and sink demand has been re-examined by Ainsworth and Bush and phloem sucrose transport has been identified as a possible target for improving plant productivity. Phloem transport capacity may not be a limiting factor, as shown in several reports.
In transgenic sugarcane, expressing a sucrose isomerase led to the accumulation of sucralose in addition to sucrose in stalk vacuoles. The sugar concentration was therefore doubled in the juice harvested from stalks Wu and Birch, In such plants, photosynthesis and sucrose transport were greatly increased, indicating a release of sink limitation.
The overexpression of an Arabidopsis tonoplastic glucose transporter TMT1 led to increased glucose contents in the vacuoles of mesophyll cells and to higher seed yield. In these plants, higher expression levels of AtSUC2 , the transporter that loads sucrose into the phloem in Arabidopsis , have been noted Wingenter et al. However, TMT1 can also drive sucrose entry into the vacuole Schulz et al. In rice, when the expression of a SUTs involved in sucrose efflux from the vacuole OsSUT2 was suppressed, seed production as well as root growth were reduced, indicating that sucrose transport to sinks was impaired Eom et al.
Altogether these different data suggest a link between the sugar concentration in the cytoplasm of mesophyll cells and the export of sucrose, and indicates source-limitation in wild-type plants.
Taking the former elements into account, source-to-sink sucrose transport can be affected by environmental factors at least at three different levels Figure 1 :. Plants undergo large changes in their environment throughout their life and have developed many strategies to respond to these changes.
The following sections will try to summarize some of the effects of environmental factors on sucrose transport from source to sink organs.
Among the many environmental factors that can affect plant growth, the present review concentrates on two types: environmental cues and some air and soil pollutants. Water deficit is a major abiotic factor affecting crop development and yield. Drought imposes unfavorable conditions on the leaves source and roots sink of a plant.
However, as pointed out by Turgeon a , the high osmotic potential in the phloem can be a positive parameter for attracting water to the sieve tubes and maintaining phloem sap flow in drought conditions. Under mild water deficit, shoot growth is restricted while root growth continues and, consequently, plant architecture is modified.
In dicots, e. In monocots such as grasses, the number of young emerging organs is reduced under drought Courtois et al. As a result of this water-stress avoidance strategy, global photosynthetic productivity may decrease and thus impact the carbon flow to different sink organs. Most research on the effect of water deficit on sugar metabolism and phloem loading has been led using sucrose-translocating species and demonstrates that in leaves, carbohydrate levels are altered by drought.
Sucrose and hexose amounts increase, while starch levels decrease Pelleschi et al. In cotton, water-stress-induced accumulation of sucrose in the source leaves has been hypothesized as providing an energy supply to maintain cell survival in high-respiration environments Burke, Furthermore, sucrose and hexose accumulation is considered to play a major role in osmotic adjustment to maintain metabolic activity in source leaves.
However, sugars may also accumulate in leaves because of a decreased demand as a consequence of growth limitation Hummel et al. The effects of water deficit on species that translocate raffinose family oligosaccharides RFOs were also investigated since RFOs are involved in desiccation tolerance in seeds Koster and Leopold, and in low-temperature acclimation of leaves Bachmann and Keller, A hypothetical model depicting the effects of water-deficit stress on the carbon flow between RFOs and O -methyl-inositol OMI has been proposed in Coleus , a drought-tolerant plant.
The two metabolic pathways share myo-inositol, a ubiquitous plant cyclitol, as an intermediate. In Coleus , the activity of galactinol synthase, an enzyme that catalyses the first step of RFO biosynthesis from UDP-galactose, was found down-regulated by water deficit, thus contributing to lower levels of transportable RFOs Pattanagul and Madore, In source leaves, transcript abundance of several genes encoding enzymes involved in gluconeogenesis such as fructose-biphosphate aldolase Cramer et al.
Transgenic Arabidopsis plants that overexpressed galactinol synthase produced elevated amounts of galactinol and raffinose, which may function as osmoprotectants and contribute to water-deficit stress tolerance Taji et al.
Such an apparent discrepancy between RFO-transporting plants such as Coleus and sucrose-transporting ones, such as Arabidopsis , may reflect differential responses of distinct species to water stress. Water deficit induces changes in the concentrations of the main organic nutrients that move inside the sieve tubes, i.
Analysis of alfalfa phloem sap, collected by stylectomy, indicated a significant increase in sucrose contents and total amino acid concentrations as the leaf water potential decreased from Similarly, water stress induced increased sucrose and Pro levels in phloem sap collected from cut petioles of Arabidopsis leaves by the EDTA method Mewis et al.
In sink organs, examples of the negative effects of drought on sink growth have been reported in potato tubers, where osmotic stress promoted sucrose biosynthesis instead of starch biosynthesis via the induction of sucrose-phosphate synthase SPS and the inhibition of ADP glucose pyrophosphorylase AGPase; Geigenberger et al.
The degradation of some storage carbohydrates such as starch and fructans in stems has been correlated to starch accumulation in grains Yang et al. Likewise, drought led to a fivefold decrease in cytosolic invertase activity in the seeds of Lupinus albus Pinheiro et al.
Data about the involvement of SUTs in drought and salinity tolerance remain limited. The authors suggest that export and long-distance sucrose transport may be at least partly controlled by SUT-mediated sucrose sequestration within the vacuole.
The effects of water deficit have also been studied at different development stages. Drought stress can induce senescence and enhance reserve mobilization Chandlee, In other terms, senescence and reserve mobilization are integral components of plant development and basic strategies in stress mitigation Cowan et al.
Studies using tomato plants over-expressing Arabidopsis hexokinase showed that increased hexokinase levels in plants induced higher sugar contents, which reduced photosynthetic activity and consequently accelerated senescence in leaves Dai et al. Sugar levels can influence leaf progress through senescence as direct causal signals, but also as substrates for carbon mobilization and reallocation to allow plants to alleviate the effects of drought stress Wingler et al.
In rice, drought-induced leaf senescence promotes allocation of assimilates to developing grains, shortens grain filling, and increases the grain filling rate Yang et al.
In soybean, water depletion decreases seed size primarily because of a shortening of the filling period rather than an inhibition of the seed growth rate Westgate et al.
Since seed growth depends on the supply of assimilates from the maternal plant source activity , as well as on the demand for assimilates within the embryonic tissues sink activity , both maternal and embryonic factors contribute to the maintenance of seed growth under water deficit.
Thus, the latter authors hypothesized that a rapid depletion of sucrose in and around the embryo would point to a source limitation, whereas a reduction in sucrose uptake would imply a sink limitation. As an example of fruit development, the ripening grape berry represents a well-characterized example of a very strong sugar sink. Grape yield is reduced under drought, while total sugar content in the surviving berries increases Huglin, The early development of grape berry appears as the most drought-sensitive stage, but in spite of negative effects on berry growth, drought does not affect sugar accumulation, confirming that sink strength within individual berries is set by sink activity, not by berry size, as reviewed by Agasse et al.
A shift from a symplastic- to an apoplastic-unloading pathway has been demonstrated. It occurs at the onset of ripening, and is accompanied by a concomitant increase of the expression and activity of cell-wall invertases, leading to a massive import of hexoses Zhang et al.
Altogether these data indicate that sensitivity to water deficit is particularly acute during reproductive development because photo-assimilate allocation to newly established sinks such as flowers, seeds, and fruit, can be compromised by competition with roots under drought stress.
In order to apply this knowledge to crop improvement, more detailed understanding of drought sensitivity at that crucial stage for productivity is needed.
Plants acquire mineral nutrients for their growth and development through the roots. Plasticity of the root system architecture is therefore a key adaptation feature that allows plants to cope with a changing environment.
As pointed out by Hermans et al. Therefore any depletion in mineral supply can have dramatic effects on resource allocation in plants. Marschner et al. As a consequence of plant growth reduction or inhibition by mineral deficiency, sugar concentrations increase in plants and in phloem sap Peuke, Response to nitrate limitation.
Scheible et al. Sugars accumulated in the leaves of N-deficient plants lead to reduced photosynthesis probably due to feedback metabolite regulation Martin et al.
Nitrogen deficiency reduces photosynthesis by a decrease in RubisCO amount and activity and also a decrease in electron transfer Paul and Driscoll, ; Antal et al.
Hermans et al. Arabidopsis microarray data suggest that genes related to primary metabolism and carbohydrate metabolism such as starch metabolism, glycolysis, and disaccharide metabolism are significantly over-represented among the differentially regulated genes in the shoots of N-deficient plants Hermans et al. All these data show that nitrogen affects the distribution of sugars across plant organs.
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. Response to phosphorus limitation.
Phosphorus is the second most limiting mineral nutrient for crop production after nitrogen. Lack of phosphorus in leaf mesophyll cells has a direct effect on photosynthesis through Pi availability in the chloroplast and leads to reduced carbon assimilation Figure 2. Nevertheless, sucrose translocation into the phloem is maintained and sometimes increased at least during the early phases of phosphorus starvation up to 6 days; Hermans et al.
Like N deficiency, phosphorus limitation induces increased photo-assimilate allocation to the roots and an adaptation of the root system architecture. Root hairs initiate and elongate in response to phosphate starvation, increasing the root surface area Hammond and White, The importance of phloem sucrose transport in P-deficiency signaling has been clearly demonstrated by Liu et al.
In white lupin roots, two genes responsible for phosphate acquisition LaPTI , a phosphate transporter and LaSAP1 , a secreted acid phosphatase are rapidly induced by phosphate starvation. When phosphate-starved plants were treated by phloem girdling to prevent shoot-to-root sucrose transport, no induction of either LaPT1 or LaSAP1 was noted. Sucrose transport from shoot to root was therefore necessary for phosphate starvation signaling.
In a search for Arabidopsis plants affected in secreted acid phosphatase activity, Zakhleniuk et al. Moreover, pho3 mutants were unable to respond further to low Pi Zakhleniuk et al. The mutation was subsequently located in the At SUC2 gene Lloyd and Zakhleniuk, and a link was thus clearly established between sucrose availability for long-distance transport and the response to P starvation.
Altogether, these data clearly demonstrate that sucrose transport to the root is a necessary signal for the response to phosphate starvation, although recent data identified miRNAs translocated into the phloem as key players in the regulation of mineral nutrition Kehr, Response to magnesium and potassium deficiency.
Metabolic processes and reactions that are influenced by Mg include chlorophyll formation, photosynthetic carbon dioxide fixation, photo-assimilate phloem loading and partitioning Cakmak and Yazici, Accumulation of carbohydrates in leaves is a common phenomenon in Mg-deficient plants Figure 2. Mg deficiency reduces leaf growth more than root growth Figure 2 and impacts on sucrose export to the roots Hermans et al. Mg deficiency is thought to affect phloem sucrose loading by decreasing Mg-ATP availability.
Therefore, changes in its amounts can have dramatic effects on phloem functions. The high sugar concentration measured in the leaves of K-deficient plants does not promote any increase in root sugar content or growth. Deeken et al. In conclusion, enhanced carbohydrate transport to the roots has been demonstrated for N and Pi limitation, but not for K or Mg deficiency Peuke et al.
Salt stress, due in many places to irrigation with poor quality water, is considered as a major factor limiting plant growth and productivity.
Salt stress shares many features with drought stress because in both cases, the primary effect is a lower soil water potential around the roots. Sodium toxicity, due to transport inside the plant via the transpiration stream, adds to that initial stress.
Little is known about the effects of salt stress on sucrose translocation into the phloem. Salt stress has an inhibitory effect on photosynthesis Suwa et al.
However, in tomato, salt stress can have a direct inhibitory effect on phloem sucrose loading and translocation, leading to a deficit in sucrose partitioning to the roots Suwa et al.
Resistance to salt stress is frequently associated with polyol-synthesizing plants as polyols are thought to act both as osmotically active and anti-oxydant molecules. When such plants are subjected to salt stress, their polyol content increases in different organs. Polyols are considered as major molecules for plants to cope with stress Stoop et al. In polyol-transporting plants, increased polyol synthesis occurs together with an increased expression of genes encoding polyol transporters located in the phloem in Plantago Pommerrenig et al.
Increased delivery of polyols to roots could have a positive effect on metabolism and water potential of roots.
Light has a direct effect on phloem loading through photosynthesis via the synthesis of sucrose and by providing energy. However, light also has an effect on the anatomy of the loading zone itself Amiard et al. Depending on the loading mode apoplastic or symplastic , the response to transfer from low light to high light and therefore acclimation to increased photosynthesis was different: in apoplastic species such as pea, cell-wall invaginations in the companion cells around the SE increased Amiard et al.
This indicated an increased exchange surface that allowed for higher sucrose phloem loading. On the contrary, in symplastic loaders such as pumpkin, plasmodesmatal frequencies did not increase, leading to starch accumulation in leaves Amiard et al.
The capacity of apoplastic loaders to increase the surface for membrane-mediated sucrose transfer around the conducting cells was further investigated Amiard et al. Besides its role in nutrient exchange, cell-wall enlargement was proposed as protecting phloem cells against pathogens and insects.
Low temperatures can affect phloem sugar transport in different ways, involving distinct cell types intermediary cells, parenchyma transfer cells, SEs. Considering that species with a symplastic minor-vein configuration dominate in tropical regions and that species with an apoplastic configuration dominate in temperate zones, temperature is considered as a major parameter of the phloem-loading mode in plants.
Symplastic loaders are considered as more cold-sensitive than apoplastic loaders Gamalei, ; Van Bel and Gamalei, Gamalei et al. However, these ultrastructural changes have not been observed in broadleaf-evergreen species Ajuga reptans , Aucuba japonica , and Hedera helix with a symplastic phloem-loading mode.
The winter leaves of these plants have a higher exudation rate at low temperatures and no starch accumulation is observed in their chloroplasts. Therefore, the removal of excessive photo-assimilates from source leaves under low temperature may be necessary to maintain their functional and structural integrity and can thus be regarded as a result of cold acclimation Hoffmann-Thoma et al.
Later physiological studies Schrier et al. This led to the hypothesis that the phloem-loading mode was related to growth architecture rather than habitat, and was confirmed by a study by Davidson et al. In monocot and dicot plant species, tocopherol vitamin E deficiency impairs photoassimilate export from source leaves via enhanced callose deposition in the vascular tissues Hofius et al.
The same effect has also been described for phloem loading under low temperature Maeda et al. Accumulation of sucrose and other soluble sugars is much higher in vte2 than in the wild-type after 60 h of low temperature treatment, although the photosynthesis and carbon fixation rates do not differ between the two genotypes. Therefore, tocopherol prevents abnormal callose deposition in phloem parenchyma cell walls and thus maintains photo-assimilate transport at low temperature.
In dicots, when short sections of stems or petioles are progressively exposed to cool temperatures thermal jackets , phloem transport stops transiently through the cooled region Faucher et al. This stoppage is local and transient as phloem transport can start again even if tissues are maintained at low temperatures Peuke et al. Furthermore, the cooling rate determines stoppage duration. In fact, the effect of cooling depends on experimental conditions and SE structure.
Conversely, in monocots, i. Further studies support the implication of sieve-element structural proteins in the cooling response Lang and Minchin, This increase only occurs if the cooling process is rapid White, The rise in carbon dioxide CO 2 in the atmosphere is suspected to be the main cause for global warming. Indeed, atmospheric CO 2 concentration increased from around ppm in to an average ppm nowadays, and predictions give a CO 2 concentration ranging between and ppm at the end of the century.
This elevated atmospheric CO 2 has a direct effect on plant photosynthesis: at the present atmospheric CO 2 concentration, the photosynthetic reaction is limited by the low affinity of the active site of RuBisCO for CO 2 in C3 plants Drake et al.
An increase in CO 2 should therefore enhance photosynthetic rates, carbohydrate production, and have a positive effect on phloem transport and growth. In fact, most of the plants grown in high CO 2 effectively exhibit increased carbohydrate accumulation in leaves with biomass partitioning between source and sink organs differing according to species Makino and Mae, Classically, two high-CO 2 acclimation steps are described, i.
Biomass formation is initially enhanced in the first days of exposure but this boosted growth is not sustained for a long time. The short-term response to high CO 2 is an acclimation process whereby net photosynthesis, net carbon assimilation and growth are enhanced Drake et al.
Excess sucrose is only partly exported to sink organs via the phloem and the resulting carbohydrate accumulation in leaves decreases the photosynthesis rate.
A comparison of sugar and starch contents in Ricinus communis leaves in plants grown at or ppm CO 2 showed that leaves accumulated starch at ppm.
Starch accumulated because more sucrose was synthesized than consumed or exported to sink organs via the phloem Grimmer et al. Phloem carbon export was induced by high CO 2 at night. In fact, R. In short, more sucrose was exported to sink organs at high CO 2. The role of increased sucrose transport as a result of increased CO 2 was also shown in Arabidopsis thaliana grown under ppm CO 2 : the plants exhibited enhanced root growth, with increased root length, root diameter and root number, and a modified branching pattern Lee-Ho et al.
The same root changes were noted on plants grown at ppm CO 2 and supplied with exogenous sucrose, confirming the role of sucrose transported from the source. After three months of CO 2 enrichment, cladodes displayed an increase in glucose, starch, and malate contents, but no change in their sucrose content was measured Wang and Nobel, However, data analysis from different plant species grown under high CO 2 shows that phloem loading cannot alone account for variations in shoot carbohydrate partitioning.
Increased CO 2 can also have negative effects on plants. Due to an imbalance in nitrate assimilation caused by high CO 2 , protein accumulation in wheat grains is low despite an unchanged yield Pleijel and Uddling, However, this is not the case for woody plants, like pine trees, which preserve seed quality while increasing seed production Way et al. Some pollutants like heavy metals, cadmium Cd , lead Pb , or mercury Hg and the metalloid arsenic As are present in soils all over the world.
Concerning Cd mobility within the phloem and its impact on sugar transport, little information is available, due to technical hurdles regarding phloem sampling Mendoza-Cozatl et al. However, a low-affinity Cd transporter, OsLCT1 , involved in phloem loading and accumulation in seeds, was identified in rice Uraguchi et al. Another experiment was led on willows used for Cd phyto-extraction. In those trees, sieve tubes and companion cells degenerated in proportion to increasing Cd concentrations supplied at the root level Vollenweider et al.
Long-distance transport was therefore impaired and a reduction in leaf size and biomass was observed Cosio et al. Phloem degeneration was also noticed on maize grown on a Cd-contaminated soil Cunha et al. Moreover, in willows, phloem regeneration was hindered due to reduced cambial activity Vollenweider et al.
Tropospheric ozone is the most widespread air pollutant in many areas of the industrialized world and the overall ozone concentration has increased over the past decades as a result of anthropogenic activities Krupa and Manning, ; Volz and Kley, Ozone mainly originates from photochemical reactions of volatile organic compounds with nitrogen oxides NOx released from anthropogenic and natural sources Stockwell et al.
Ozone causes a series of negative effects on vegetation such as decreased photosynthesis and growth, enhanced premature senescence and reduced crop yield Pell and Dann, ; Sandermann, O 3 alters chloroplast membranes and decreases photosynthesis by reducing RuBisCO activity and concentration Grams et al. Thus the availability of photo-assimilates for sink organs is decreased Fiscus et al. Grantz and Yang tried to understand whether the impact of O 3 on reduced carbon allocation in plants was due to source limitation or inhibition of translocation.
The results indicate that ozone has direct effects on phloem transport with consequent inhibition of translocation to roots, as previously suggested by Mortensen and Engvild These data are consistent with a primary effect on phloem loading and secondary feedback inhibition of photosynthesis Grantz, ; Grantz et al. The results show that both parameters were significantly reduced by ozone but k showed more variability than RGR.
This could indicate that root allocation is disturbed by O 3 but photo-assimilate availability is not. This result is consistent with an inhibition of photo-assimilate translocation rather than with a limitation of the photosynthetic process Grantz et al. Carbon translocation from source leaves of Pima cotton has been directly studied by monitoring 14 C-labeled photo-assimilates during a sudden exposure to O 3.
Another study examined the translocation velocity of 14 C-labeled photo-assimilates in wheat : although the authors observed no significant difference in the translocation velocity in O 3 -treated plants, the amount of carbon transported decreased Mortensen and Engvild, In conclusion, O 3 could induce changes in carbon allocation or partitioning probably due to decreased amounts of transported carbon. All those works highlight that the major impact of ozone is the reduction of phloem loading probably linked to oxidant damage on plasmalemma or plamodesmata in mesophyll or phloem companion cells Grantz and Farrar, O 3 exposure could also have an indirect effect on plants by blocking phloem translocation via the induction of callose deposition on phloem sieve plates Wilkinson et al.
In potato, accumulation of callose in the phloem and starch in the parenchyma cells of source leaves was observed after ozone exposure. O 3 also decreased tuber weight, supporting the hypothesis of impaired phloem functioning Asensi-Fabado et al. A better understanding of the effects of O 3 on carbohydrate translocation could come through the study of apoplastic and symplastic phloem-loading species to confirm the oxidant impact of O 3 on membranes Grantz and Yang, SO 2 is highly soluble in water: a concentration of 0.
The pollutant can accumulate in leaf tissues and cause disturbances in physiological mechanisms such as photosynthesis, respiration, transpiration Saxe and Murali, In bean leaves Minchin and Gould, and castor bean cotyledons Lorenc-Plucinska and Ziegler, , photo-assimilate translocation is also affected due to inhibited phloem loading, independently of reduced photosynthesis.
During their development, plants have to deal with the presence of microbes, like fungi, viruses, bacteria and also herbivores and sometimes other plants that act as parasites.
Those organisms, whatever their type, develop at the expense of the sugars produced by plants Figure 3 , and may therefore affect phloem transport of sugars.
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. 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.
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.
Microorganisms can be separated into two groups according to their lifestyles, mutualistic e. Even if their modes of colonization are different, microorganisms have evolved sophisticated strategies to avoid, suppress or bypass plant defenses and to divert nutrients, especially sugars, from the host plant for their growth Figure 3. For example, mutualistic microorganisms and biotrophic pathogens can grow within the plant through complex interfaces, arbuscules and haustoria respectively, through which nutrients are transferred Voegele and Mendgen, ; Smith and Smith, In contrast, necrotrophic pathogens secrete toxins and produce hydrolytic enzymes that kill host cells in order to feed on macerating tissues van Kan, Microbes can colonize either sink or source organs.
Because both mutualistic and pathogenic interactions require sugar supply from host plants to the heterotrophic colonizing agent, they interfere with the source-sink balance.
In most cases, it is largely assumed that colonized source organs are subjected to a source-to-sink transition that modifies the mechanism of sugar transport and partitioning at the whole plant level Biemelt and Sonnewald, Among pathosystems, interactions between plants and biotrophic fungi are often cited as models for the study of pathogen-related modifications of carbon partitioning.
For this reason, we particularly focus here on plant-biotrophic fungus interactions and only mention a few distinctive features of other pathosystems. Biotrophic fungi, e. These are penetrating cell-wall structures that leave the protoplast of host cells intact and create an apoplastic interface through which released host nutrients are absorbed by the fungus Mendgen and Hahn, ; Panstruga, Autoradiography studies using radiolabeled substances give indirect evidence for the central role of haustoria in sugar and amino-acid transfer from host to biotrophic pathogens Hall and Williams, ; Voegele and Mendgen, In infected tissues, the fungal carbon demand creates an additional major sink that competes with host sinks.
Competitiveness between plant and fungal sinks has been recently examined using a combined experimental-modeling approach. The authors showed that, in wheat infected by the leaf rust fungus Puccinia triticina , fungal sporulation had a competitive priority for photo-assimilates over grain filling Bancal et al.
The nature of the host carbon energy source hexoses or sucrose transferred through the haustoria has been a matter of debate as to the origin of the apoplastic sugars taken up Figure 3. Rather than sucrose, glucose appears to be the major carbohydrate imported from the host to the parasite, e.
Apoplastic sucrose is most likely hydrolysed by cell-wall invertases cwINV which are key players in supplying carbohydrates to sink tissues Roitsch and Gonzalez, Many studies report increased invertase activity in response to powdery mildew or other pathogens and in different plant species Roitsch et al. This increase in cwINV activity in infected tissues constitutes a major driving force in sugar unloading. For most pathosystems, especially with obligate pathogens, it is difficult to discriminate between plant or pathogen contribution to the induced cwINV activity Figure 3.
So far few studies have reported fungal cwINV involved in such activities. The characterization of rust fungus Uromyces fabae Uf-INV1 suggests a fungal contribution to the higher cwINV activity in the biotrophic interaction with the host plant Vicia faba Voegele et al.
Regarding the necrotrophic parasite Botrytis cinerea , a contribution of the fungus to higher cwINV activity during infection of Vitis vinifera has been evidenced Ruiz and Ruffner, Accordingly, both partners appear to activate their own invertases, providing strong support to the theory that infection by pathogens creates a new sink that competes with existing sinks Figure 3.
As a consequence, hexoses accumulate in the apoplast, and are taken up by co-regulated hexose transporters Wright et al. High extracellular sugar levels are somehow beneficial for both partners. On the plant side, sugars act as signaling molecules that can regulate many physiological processes, including defense mechanisms through the control of gene expression Herbers et al.
For example, sugars induce pathogenesis-related genes and repress photosynthetic genes Roitsch, ; Bolouri Moghaddam and Van den Ende, An indirect host defense strategy consists in starving the pathogen by limiting host sugar availability at the interface. Reports describe an increased capacity for glucose retrieval by host tissues after challenge by biotrophic as well as necrotrophic pathogens Fotopoulos et al.
Some plant monosaccharide transporters MSTs are involved in sugar resorption upon infection Buttner, ; Slewinski, Further molecular evidence of a competition for apoplastic glucose has been provided in infected broad bean by the identification and characterization of rust Uromyces fabae sugar transporter UfHXT1, which is localized in the haustorial plasma membrane. UfHXT1 preferentially transports glucose and fructose rather than sucrose to the fungus Voegele et al.
Substrate specificity and localization of such fungal MSTs facilitates plant hexose assimilation and thus participates in fungal sink strength Figure 3. Mutualistic or pathogenic microorganisms use a wide range of different strategies to gain access to carbohydrates from host plants, as highlighted in Figure 3. Mycorrhizal fungus Glomus high-affinity MST2 has been identified as a major player in sugar uptake with a critical function in the establishment of symbiosis Helber et al.
Five hexose transporters CgHXT have been characterized in the maize hemibiotrophic pathogen Colletotrichum graminicola , with large substrate specificities. CgHXT genes are differentially expressed during all infection phases, whether biotrophic or necrotrophic Lingner et al. Roles for fructose as a potent inducer of fungus germination have been suggested Doehlemann et al.
Sucrose is the main photo-assimilate translocated from source to sinks. Upon release from the phloem in sink organs, sucrose is unloaded into the apoplast and is potentially exploitable by the fungus.
In infected tissues, apoplastic sucrose uptake by fungal cells is believed to require the presence of fungal SUTs localized in the haustorial structure. The identification of SRT1, a highly specific SUT from the corn smut fungus Ustilago maydis , suggests that this fungus can efficiently use apoplastic sucrose Talbot, ; Wahl et al. Ustilago maydis hyphae grow along the phloem of infected maize plants where they have access to sucrose released from the phloem.
Such a transporter i. The identification and characterization of other fungal SUTs is not yet achieved and constitutes an open field to better understand the competition for sugars that takes place between the plant and the fungus Doidy et al. Recently, key insights into how microbes acquire the ability to use the host sugar efflux machinery for nutrient supply have been gained thanks to the discovery of a new class of plasma membrane-localized sugar transporters Figure 3.
SWEETs were at first identified as glucose uniporters but paralogues i. Different patterns of expression have been reported after challenge by either bacterial Pseudomonas syringae pv tomato strains or fungal the necrotroph B.
Authors also described a model in which OsSWEET11 and 14 expression is specifically targeted by Xanthomonas oryzae pv oryzae effectors to increase sugar efflux into the apoplast Chen et al. Both specific bacterial effectors and OsSWEET expression are required for bacterial virulence, suggesting that pathogens probably take advantage of the SWEET-induced sugar efflux mechanism to gain access to sugars in cells around the infection site in order to support their own growth.
The identification of this non-conventional family of sugar transporters highlights additional complexity and opens new perspectives onto our knowledge about sugar partitioning during plant-pathogen interactions. Among plant pathogens, viruses are unique because they remain exclusively in the symplast of their host Schoelz et al.
This mode of colonization requires viruses to move from infection site to systemic tissues via the symplastic continuity created by cell-to-cell connections plasmodesmata, PD and the phloem long-distance translocation system Lucas and Wolf, ; Gosalvez-Bernal et al.
Viral infection involves virus-encoded movement proteins MPs which alter the exclusion size of PDs, suggesting that viruses can exploit the PD-mediated cell-to-cell trafficking of photo-assimilates. Carbohydrate allocation and signaling can be directly affected during virus infection.
The mechanisms of these metabolic changes caused by viral infection have been assessed using transgenic expression of viral MPs; Olesinski et al. Plants expressing viral MPs exhibited dilated PDs associated with significant physiological alterations such as changes in host primary metabolism, accumulation of starch and soluble sugars, decreased photosynthesis and increased respiration Tecsi et al. These changes strongly suggest that virus-infected leaves function as sinks.
However, the effects of viral MPs on carbohydrate allocation can vary according to the way viruses exploit the host transport system. In some cases, it is not related to the PD size exclusion limit, but may rather be due to induced callose deposition at the PD level which consequently blocks symplastic sucrose transport Biemelt and Sonnewald, Virus-induced reallocation of host resources and its mechanisms seem to be virus-specific and result from interactions between specific viral and host components Culver and Padmanabhan, For example, in Cucumber Mosaic Virus CMV -infected melon, modifications in phloem sap sugar composition, such as an increase in sucrose content, have been reported Shalitin and Wolf, Aphids, which are the vectors of numerous plant viruses Brault et al.
Using fine stylets, they drill into tissues intercellularly, making tiny punctures, and wait a few seconds to analyze the physicochemical properties of the microenvironment around the stylet tip Tjallingii, Experiments using artificial systems indicate that the ability of aphids to find sieve tubes is linked to their ability to sense high sucrose concentrations and pH Hewer et al.
Aphids constitute an additional sink that can modify assimilate allocation at the whole plant level, especially at the expense of the stem apex Hawkins et al. Data from various controlled infestations of alfalfa stems by pea aphids indicate that the reduction of the stem elongation rate SER is only partly explained by assimilate withdrawal and suggests that extra signals associated to pea aphid probing and feeding are involved in SER reduction Girousse et al.
In addition, dramatic changes in carbon and nitrogen allocation were observed under growth-chamber conditions using severe and short-time aphid infestations. Because this process involves building bonds to synthesize a large molecule, it requires an input of energy light to proceed. The synthesis of glucose by photosynthesis is described by this equation notice that it is the reverse of the previous equation :.
In plants, glucose is stored in the form of starch, which can be broken down back into glucose via cellular respiration in order to supply ATP. Learning Objectives Analyze the importance of carbohydrate metabolism to energy production.
Metabolism of Carbohydrates Carbohydrates are one of the major forms of energy for animals and plants. Figure: All living things use carbohydrates as a form of energy. Both plants and animals like this squirrel use cellular respiration to derive energy from the organic molecules originally produced by plants. Energy Production from Carbohydrates Cellular Respiration The metabolism of any monosaccharide simple sugar can produce energy for the cell to use.
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