The production of carbohydrates via photosynthesis is the most fundamental activity in plant life. Carbohydrate synthesis, transport, utilization, and storage are dynamic processes, strongly dependent on cell physiology, plant organ, environmental conditions, and developmental stage of the plant. The plant’s ability to monitor and respond to the level of carbohydrates may act as a controlling mechanism, integrating the influence of environmental conditions (e.g. light, nutrients, biotic and abiotic stress factors) with internal developmental programs, controlled directly by hormones (Koch 2004, Rolland et al. 2006, Hammond and White 2008, Loreti et al. 2008, Ramon et al. 2008, Agulló-Antón et al. 2011). Studies conducted in recent years have provided an extensive body of information on the participation of carbohydrates in metabolic reactions of plant cells. In plants, sugars are essential as respiratory substrates for the generation of energy and metabolic intermediates that are then used for the synthesis of macromolecules. Binding to sugar is required for proper functioning of many proteins and lipids. Moreover, carbohydrates have important hormone-like functions as physiological signals, which cause activation or repression of many plant genes, and this in turn leads to specific metabolic effects. Sugar-signaling networks have the ability to regulate directly the expression of genes and to interact with other signaling pathways. The progress in research on molecular mechanisms of sugar sensing and signaling in plants shows that signal molecules include glucose, fructose, sucrose, and trehalose (Jang and Sheen 1994, Koch 1996, Müller et al. 1999, Rolland et al. 2002, Koch 2004, Gibson 2005, Gonzali et al. 2006, Rolland et al. 2006, Ramon et al. 2008, Rosa et al. 2009, Cho and Yoo 2011). Plants have developed effective mechanisms of perception and transduction of sugar signals. Perception of the sugar signal may take place already in the apoplast during transport across membranes or within the cell, in the cytosol. Sugar signal perception and transduction may involve cell wall invertases (CW-INV), sucrose and glucose transporters (and specific sugar receptors), and hexokinase (HXK) (Sheen et al. 1999, Smeekens 2000, Loreti et al. 2001, Rolland et al. 2002, Harrington and Bush 2003, Moore et al. 2003, Sherson et al. 2003, Koch 2004, Rolland and Sheen 2005, Rolland et al. 2006, Ramon et al. 2008, Cho et al. 2009, Hanson and Smeekens 2009, Smeekens et al. 2010). Additionally, biochemical studies provide evidence for the involvement of a variety of protein kinases, i.e. Snf1-related kinases (SnRKs) (Rolland et al. 2006, Smeekens et al. 2010), calcium-dependent protein kinases (CDPKs), mitogen-activated protein kinases (MAPKs), and protein phosphatases, 14-3-3 proteins, Ca2+ ions as a second messenger, and G-proteins (Rolland et al. 2006) in sugar signal transduction (Rolland et al. 2002, Sinha et al. 2002). However, it must be stressed that HXK plays a significant role as a component of the sugar sensing machinery. Genetic analyses have revealed a central role for HXK as a conserved glucose sensor (Moore et al. 2003, Harrington and Bush 2003, Rolland and Sheen 2005, Rolland et al. 2006, Ramon et al. 2008, Cho et al. 2009, Hanson and Smeekens 2009, Smeekens et al. 2010). HXK sensing and signaling functions are probably dependent on HXK’s subcellular localization, translocation, and/or interactions with downstream effectors. The HXK sugar sensor, as a cytosolic protein or associated with mitochondria or other organelles, then could activate a signaling cascade through HXK-interacting proteins (HIPs) or affect transcription directly after nuclear translocation (Rolland et al. 2002, Rolland et al. 2006, Hanson and Smeekens 2009). Various sugar signals activate many HXK-dependent and HXK-independent pathways and use different molecular mechanisms to control transcription, translation, protein stability, and enzymatic activity. It has been shown that in 7-day-old
Genes encoding the enzymes of the phenylpropanoid biosynthesis pathway (Hara et al. 2003, Solfanelli et al. 2006, Morkunas et al. 2011) as well as sink-specific enzymes, such as sucrose synthase (Salanoubat and Belliard 1989), granule-bound starch synthase (Visser et al. 1991), and extracellular invertase (Roitsch et al. 1995), are induced by sucrose or glucose. Sugar-induced gene expression has also been detected for enzymes involved in pathogen and stress response, such as proteinase inhibitor II of potato (Johnson and Ryan 1990), chalcone synthase (Tsukaya et al. 1991), and flavonoid biosynthetic enzymes (Morkunas et al. 2011). In contrast, sugar repression of photosynthetic genes was observed. For example, genes encoding photosynthetic proteins, e.g. the small subunit of the Calvin cycle enzyme ribulose bisphosphate carboxylase/oxygenase (Rubisco) and the chlorophyll
Due to their regulatory and signal function, sugars affect all phases of the plant life cycle by controlling the number of essential metabolic processes. In animals, the level of sugar in cells is strictly controlled, but in plants the level and composition of carbohydrates varies widely, depending on tissue type and environmental conditions. An excess or loss of carbohydrates or their derivatives triggers various reactions in plants and significantly affects the metabolism, growth, and development. Moreover, all abiotic and biotic stress responses are regulated, at least in part, by sugars (Koch 1996, Rolland et al. 2002). Plants are generally considered to be autotrophs but sometimes they can be heterotrophs, e.g. at some stages of development (such as seed germination, as long as the seedling grows in darkness, before it emerges above the soil surface) and in non-photosynthetic organs, such as most roots, stems, and flowers. In germinating seeds, in periods of unfavorable environmental conditions or after too deep sowing, mobilization of storage materials in cotyledons may be delayed or there may be some disturbances in distribution of carbohydrates. This may lead to a decrease in available carbohydrates in embryo axes (i.e. sugar starvation) and in a lower seed germination rate. Additionally, high carbohydrate losses can be observed in most plant species under the influence of environmental conditions, such as water or temperature, attack of pathogens or herbivores. These factors may lead to a remarkable decrease in photosynthetic rate in donor tissues (i.e. leaves that synthesize and export carbohydrates), and this reduces the supply of carbohydrates to acceptor tissues (i.e. non-photosynthetic tissues importing carbohydrates for respiration, growth, and development). Besides, in some conditions, e.g. during dormancy or leaf shedding, photosynthesis is switched off or slowed down. In such conditions, the stored carbohydrates must be used, so their reserves may be greatly diminished in non-photosynthetic tissues then. Knowledge of the response to sugar starvation and of adaptive mechanisms in plants is both fundamental and agronomically important.
2. Materials and methods of research on sugar starvation
Carbohydrate starvation has been studied in many of plant species, e.g. in common wheat (Wittenbach 1977, Wittenbach et al. 1982), maize (Saglio and Pradet 1980, Pace et al. 1990), barley (Farrar 1981), pearl millet (Baysdorfer et al. 1988), pea (Webster and van’t Hof 1973, Sahulka and Lisa 1978, Webster and Henry 1987, Morkunas et al. 1999, 2000), soybean (Kerr et al. 1985, Walsh et al. 1987), sycamore (Journet et al. 1986, Dorne et al. 1987, Roby et al. 1987, Genix et al. 1990), tobacco (Moriyasu and Ohsumi 1996), lupine (Morkunas et al. 1999, Borek and Ratajczak 2002, Morkunas et. al. 2003, Borek et al. 2006, Borek and Nuc 2011, Borek et al. 2011, 2012a, 2012b),
Particularly valuable information is obtained as a result of research on various types of mutants, which sometimes supplies surprising information about the role of sugars as signal molecules (Gibson 2005, Ramon et al. 2008, Usadel et al. 2008, Hanson and Smeekens 2009).
Plant reactions to sugar deficits have been studied with the use of a wide range of research methods: electron microscopy (Borek and Ratajczak 2002, Borek et al. 2006, 2011, 2012a), confocal microscopy (Morkunas and Bednarski 2008, Morkunas et al. 2011, 2012), enzymatic activity assays and metabolite assays, e.g. by using HPLC (Morkunas et al. 2010), nuclear 1HNMR spectroscopy (Brouquisse et al. 2007, Kim et al. 2007), and 13C and 31P-NMR spectroscopy (Vauclare et al. 2010, Gout et al. 2011). Electron paramagnetic resonance (EPR) spectroscopy is applied to measure free radicals (Morkunas et al. 2004, Morkunas and Bednarski 2008, Morkunas et al. 2008, 2012). Novelties include various methods of molecular biology: assays of gene expression (Buchanan-Wollaston et al. 2005) and application of reporter genes (Lee et al. 2007). Moreover, sugar-starvation-induced promoters have been used to obtain useful recombinant proteins (Xu et al. 2011a, 2011b).
3. Morphological, anatomical, and ultrastructural changes under sugar starvation
Sugar starvation causes changes in growth, as shown in organ cultures
Light micrographs of radicle cross sections revealed that starved radicles were thicker than sugar-fed radicles. Cortical cells of sugar-fed embryo axes were rounded, with large intercellular spaces. Many of the observed cells were dividing or have just divided. The cells lacked a central vacuole; instead, they contained very numerous small vacuoles. The major feature distinguishing cortical cells of starved lupine (as compared to sugar-fed lupine) was the presence of a large central vacuole with marginal cytoplasm.
Ultrastructural studies of the root meristematic zone of sucrose-starved lupine embryo axes showed that (in contrast to cells of embryo axes fed with sucrose) their cytoplasm, along with endoplasmic reticulum, mitochondria, plastids, ribosomes, and nuclei, were forced to the periphery by growing vacuoles (Fig. 1A, B). In spite of gradual autolysis of cytoplasmic proteins, in starved cells mitochondria were protected as organelles maintaining cellular respiration. Electron micrographs reveal that the inner mitochondrial membrane in starved pea cells is well developed, forming numerous cristae (Fig. 2A), in contrast to sucrose-fed cells, with less developed cristae (Fig. 2B). Oxygraphic studies of mitochondria isolated from starved embryos of
Research conducted on
4. Plant metabolism under sugar starvation
The studies have shown that in most cases, sugar starvation triggers a specific sequence of events in plant cells. The cells subjected to sugar starvation at first adapt to the lack of carbohydrates through gradual replacement of carbohydrate metabolism by protein and lipid metabolism. Such metabolic reorganization may result in autophagy (Saglio and Pradet 1980, Journet et al. 1986, Brouquisse et al. 1991, Rose et al. 2006). Brouquisse et al. (1992) report that during sugar starvation of maize root meristems, 3 phases can be distinguished:
acclimation (from 0 to 30-35 h), when cellular carbohydrate levels and respiration rate decrease, while nitrogen is released from storage proteins through their degradation;
survival phase (from 30-35 to 90-100 h), involving intensive breakdown of proteins and lipids, release of Pi phosphorylcholine, and free amino acids; this phase can be reversed by sugar feeding;
cell disorganization (more than 100 h), when the level of all metabolites and enzymatic activity are significantly decreased and the changes are irreversible, leading to death.
During sugar starvation at the acclimation and survival phases, the total protein content decreases. This is associated with a temporary increase in free amino acids and an increase in proteolytic activity (Tassi et al. 1992, James et al. 1993, Moriyasu and Ohsumi 1996, Borek and Ratajczak 2002).
A perfect example of enzymes induced under sugar starvation is glutamate dehydrogenase (GDH). This is a mitochondrial enzyme that catalyzes the synthesis and degradation of glutamate, which is one of the central amino acids of nitrogen metabolism in plants (Lehmann and Ratajczak 2008, Borek et al. 2011). The reversibility of the reaction catalyzed by GDH
The higher activity of the enzymes of protein and amino acid catabolism under sugar starvation probably results from the release of the genes encoding them from catabolite repression (caused by sugar). Catabolite repression is of fundamental importance since it allows cells to adapt their metabolism to carbon sources other than sugar when they are in a habitat where sugar is unavailable. If sugar is present in the medium, then the synthesis of enzymes of the catabolism of carbon sources other than carbohydrates is inhibited. This applies to proteolytic enzymes, amino acid dehydrogenases (mostly GDH), alcohol dehydrogenase, and isocitrate dehydrogenase. Other studies of the influence of sugar deficit on plant cell metabolism show that already in the initial phase of starvation (after 1.5 h), specific proteins appear, known as carbohydrate-responsive proteins (Baysdorfer et al. 1988). They may be the proteins associated with the phase of tissue acclimation to sugar starvation. Prolonged starvation results in synthesis of many specific proteins known as starvation-related proteins (STP) (Tassi et al. 1992). The genes encoding them (at least some of them) are normally under catabolite repression caused by carbohydrates. Their expression is initiated when the level of sugar in the cell falls below a critical level.
During sugar starvation, respiration rate declines rapidly in embryos of garden pea (Morkunas et al. 2000) and yellow lupine (Borek et al. 2011). The lower respiration rate is caused by the deficit of respiratory substrates rather than by mitochondrial degradation. In mitochondria isolated from starved pea embryos, respiratory activity (with glutamate as a substrate) is 60% higher than in those isolated from embryos fed with 60 mM sucrose (Morkunas et al. 2000). A similar relationship was observed in mitochondrial fractions from starved and control (sugar-fed) embryos of narrowleaf lupine (Morkunas et al. 2003). The concentration of mitochondrial proteins in starved cells was slightly lower than in control cells, and the activity of a mitochondrial marker enzyme, NAD+-dependent isocitrate dehydrogenase, was reduced in starved embryos only slightly. Besides, mitochondria isolated from lupine embryo axes cultivated without sucrose, exhibited respiration coupled with oxidative phosphorylation. They exhibited a respiration control ratio of 2 for succinate as a respiratory substrate. Mitochondria isolated from starved embryo axes oxidized glutamate and malate more intensively than mitochondria from embryo axes fed with sucrose. Ultrastructural analysis of cells of starved pea embryo axes shows that the inner mitochondrial membrane is highly convoluted, forming many folds (cristae, Fig. 2A). A similar finding was reported by Journet et al. (1986) who studied sycamore cell suspension. Mitochondria were protected in sycamore cells even as late as after 60 h of starvation, and then an addition of sugar to the medium resulted in intensive respiration. In starved cultures, sugar reserves were used up very quickly. Respiration rate was maintained at a high level for up to 30 h of starvation. In that period, respiratory substrates were provided by degradation of starch, phosphate esters, and proteins. Morkunas et al. (2000) also showed that the transfer of pea embryo axes from sugar starvation conditions onto the medium with sucrose after 48 h recovered their respiration activity. Metabolic adaptations of starved embryos of lupine (Morkunas et al. 2003) and pea (Morkunas et al. 2000) were quite effective physiologically, enabling their survival, and their transfer to a medium with sucrose allowed restoration of normal growth. Similarly, Couée et al. (1992), who studied maize root tips cultured
Under sugar starvation, the increased utilization of cytosolic proteins and storage proteins, is accompanied by a more intensive catabolism of lipids, aimed to supply respiratory substrates. In turn, sugar feeding significantly retards the breakdown of storage lipid. In the research on the regulatory function of sugars in lipid metabolism, sucrose and glucose are predominantly taken under consideration. Sucrose is particularly important in seed tissues because storage lipid is synthesized from this sugar in developing seeds and sucrose is one of the main end products of storage lipid breakdown during seed germination. In seedlings of
Transcriptome analysis of sucrose-starved rice suspension cells has revealed a decrease in the expression of transcripts involved in fatty acid synthesis but induced those involved in fatty acid degradation, such as 3-ketoacyl-CoA thiolase, fatty acid multifunctional proteins, and acyl-CoA oxidase (Wang et al. 2007). An increased expression of genes encoding lipase and enzymes linked to fatty acid β-oxidation was noted in sucrose-starved
Another set of data concerns the regulation of lipid metabolism by sucrose in developing and germinating protein lupine seeds (storage protein content up to 45% of seed dry matter). Restriction in sucrose feeding of developing embryos of yellow lupine (lipid content about 6% of seed dry matter), white lupine (lipid content 7-14%), and Andean lupine (lipid content about 20%) caused a decrease in storage lipid accumulation during seed development (Borek et al. 2009). Ultrastructural investigations of cotyledons of 4-day-old yellow, white, and Andean lupine seedlings showed that oil bodies were smaller and less numerous when sugar level was decreased in tissues (Borek et al. 2006, 2011, 2012a). A peculiar and puzzling feature was observed in 4-day-old sucrose-starved isolated embryo axes of yellow, white, and Andean lupine grown
5. The role of sugar starvation in plant growth and development
As mentioned above, sugar in plants is not only an energetic and structural substrate but it also regulates the expression of many genes. Sugar may play a role of hormonal-like signal in a variety of eukaryotic cell types. The best known are the signaling pathways in yeasts (
Most of the data on the regulatory role of sugar starvation in plant development was obtained as a result of research on senescence of plant organs, particularly of leaves and flowers. Controversies between groups of researchers on the role of sugar in leaf senescence may partly result from selection of various experimental models. Buchanan-Wollaston et al. (2005) identified over 800 genes of
There is also a rich literature on participation of the sugar signal in mobilization of storage materials during seed germination. Interaction between sugar and gibberellin in germinating barley grain is well documented (Thomas and Rodriquez 1994). Depending on the seedling’s demand for carbohydrates, the rate of starch mobilization in barley endosperm is regulated by a combination of the sugar signal with gibberellin. This regulation is a textbook example of the role of feedback in metabolic adaptation to developmental needs of the plant (Bewley and Black 1994). Results of research on the role of sugar starvation in the expression of amylase genes have some practical applications. Promoter of the gene of rice α-amylase 3D (RAmy3D), which is induced by sugar starvation, has proved to be very useful in transgenic plant cell cultures producing recombinant proteins, including plant-made pharmaceutical and plant-made industrial proteins (Park et al. 2010, Huang and McDonald 2012). For example, this promoter has been used for achieving high-level expression in rice cell suspension cultures of many therapeutic proteins, including human growth hormone, human α1-antitrypsin, human granulocyte-macrophage colony stimulating factor, bryodin-1, lysozyme and human serum albumin (Xu et al. 2011a, 2011b). Virtually every recombinant protein expressed in this rice suspension cell system has produced significantly higher secreted protein levels than attained with any other plant cell expression system tested (Xu et al. 2011a).
The role of sugar starvation in the control of storage lipid mobilization in germinating seeds was mentioned above. Storage protein mobilization in germinating seeds is also affected by sugar starvation. A good model for research on this phenomenon is yellow lupine seed. Its main storage compounds are proteins, which account for up to 45% of seed dry weight (Duranti et al. 2008, Borek et al. 2012a, 2012b). In ripe lupine seeds, starch is absent (Duranti et al. 2008, Borek et al. 2006, 2011). Sugar starvation releases from catabolite repression not only the genes of proteolytic enzymes but also the genes of amino acid catabolism. This allows the use of amino acid carbon skeletons both as sources of energy and as structural components. Interestingly, transitional starch appears during germination of yellow lupine seeds both in cotyledons and in seedling embryo axes (Borek et al. 2006, 2011, 2012a). This phenomenon can be explained by analogy with the appearance of transitional starch in leaves during photosynthesis. Sugar signal inhibits the expression of genes of some photosynthetic proteins (Sheen 1990, Krapp et al. 1993), so carbohydrates must be quickly converted into the neutral starch. In cotyledons of germinating lupine, carbohydrates are synthesized through gluconeogenesis (Borek et al. 2003, Borek and Ratajczak 2010, Borek et al. 2011), so transitional starch synthesis prevents the inhibition by sugar of the continued mobilization of storage lipids and proteins. Transitional starch synthesis in seedling embryo axes may help to maintain the gradient necessary for sugar transport between the source (cotyledons) and the sink (embryo axes). Hypocotyl elongation of etiolated seedlings was suppressed by sugar. However, it is possible that maintenance of an appropriate level of carbohydrates in the embryo axis prevents the inhibition of hypocotyl elongation in etiolated seedlings (Jang et al. 1997, Rolland et al. 2002, Yang et al. 2004, Borek et al. 2012a). The major task of the hypocotyl during epigeal germination (e.g. in lupine) is to bring the cotyledons above the ground. Thus excessively deep sowing may lead to a loss of the ability to transform cotyledons from storage materials into photosynthetic organs (Elamrani et al. 1994).
Sugar signal in cooperation with hormone signaling pathways, may control a wide range of processes related to plant growth and development (Rolland et al. 2006). Sugar and nitrogen are the main factors that modify plant morphology, as they determine the growth rate and transition to the next developmental stages. Transcription analyses show that sugar and inorganic nitrogen act as both metabolites and signaling molecules (Price et al. 2004). There are many recent reports about the role of sugar starvation in processes of shoot growth reduction and root proliferation enhancement during phosphorus deficits (Ciereszko et al. 2005, Karthikeyan et al. 2007, Polit and Ciereszko 2009). The importance of sugar in plant responses to biotic and abiotic stresses is discussed in section 7.
6. Sugar starvation versus senescence
Shaded leaves age more quickly. Their sugar content declines as a result of limited photosynthesis, so their senescence may be induced by sugar starvation. Chung et al. (1997) discovered in
As in the case of leaf senescence, there is some controversy about the role of sugar starvation in flower senescence. Sugar starvation may be involved in the process of flower senescence because application of sugars to cut flowers generally delays its visible symptoms (van Doorn 2004). However, petals showing symptoms of senescence have a relatively high sugar content. Arrom and Munné-Bosch (2012) assayed a large number of sugars and hormones in various organs of uncut and cut lily flowers. Addition of sucrose to the vase solution elevated the level of sugar in various organs of cut flowers, but primarily it altered the hormonal balance of floral tissues. Those results confirm the earlier findings that sucrose added to the vase solution accelerates the senescence of cut flowers with the participation of hormones. Hoeberichts et al. (2007) used cDNA microarrays to characterize senescence-associated gene expression in petals of cut carnation (
At the cellular level, sugar starvation in senescent organs and in organs that have not initiated the senescence program causes similar or identical symptoms: degradation of cellular structures and degradation of many cellular components, such as proteins and lipids. Nevertheless, the goals of these transformations differ. In the case of senescence, valuable metabolites are removed from the cells destined to die, to feed other cells in other plant organs, e.g. in developing leaves or maturing seeds. During sugar starvation of non-senescent organs, protein and lipid degradation is aimed to supply substrates for respiratory processes, which provide the energy necessary for survival. Senescence is a stage of programmed death, during which a low level of sugar may be necessary for activation of some senescence-associated genes, whose expression is repressed by sugar. However, sugar starvation can be used in plant development in many other processes, not only in programmed cell death. As mentioned above, sugar signaling may, in cooperation with plant hormones, play a major role in plant response to environmental factors and in shaping of plant morphology. However, even at the level of cells, sugar starvation, if not associated with programmed cell death, may show other symptoms than during senescence. For example, generation of free radicals (which play an important role in programmed cell death) may be neutralized by initiation of scavenging free radicals whenever cells need to be protected against the negative effects of sugar starvation (Morkunas et al. 1999, 2003). The role of sugars in plant defense response against free radicals is discussed in section 7.
7. Effect of sugar starvation on plant response to biotic and abiotic stress factors
Depending on the duration of sugar starvation, considerable ultrastructural and metabolic changes were observed in plant cells (see above). Moreover, it was interesting whether sugar starvation (as a nutritional stress) is accompanied by changes in the redox status of the cell, like in the case of plant response to other stress factors (biotic and abiotic). In plant response to abiotic stress factors, the increased generation of free radicals, including reactive oxygen species (ROS), attests to a greater influence of the stress factor, whereas during the plant-pathogen interaction, particularly at an early stage of the infection, an increased generation of free radicals in plant cells is favorable (Morkunas and Bednarski 2008). Free radicals may be toxic to the pathogenic microorganism, hamper the penetration of host tissues (through initiation of lignification of host cell walls), activate the expression of host defense genes, and participate in signal transduction over short and long distances.
Under sugar starvation, synthesis of free radicals is intensified, particularly after 72 and 96 h of starvation of lupine embryo axes
Apart from the well-known classical antioxidant mechanisms, sugars and sugar-metabolizing enzymes are important players in the defense against oxidative stress (Bolouri-Moghaddam et al. 2010). Those authors hypothesized that the synergistic interaction of sugars (or sugar-like compounds) and phenolic compounds is a part of an integrated redox system. It quenches ROS and contributes to stress tolerance, especially in tissues or organelles with high soluble sugar concentrations.
Moreover, sugar-signaling pathways interact with stress pathways in a complex network, which modulates metabolic plant responses (Ho et al. 2001, Tran et al. 2007). Soluble sugars may either act directly as negative signals or as modulators of plant sensitivity, so they can also play important roles in cell responses to stress-induced remote signals (Rosa et al. 2009). Descriptive ecological and agronomic studies have revealed a strong correlation between soluble sugar concentrations and stress tolerance. However, since energy and resources are required for plants to cope with abiotic and biotic stress conditions, the source-sink partitioning between different organs is a crucial component of the mechanisms of stress tolerance (Ho 1988, Krapp and Stitt 1995). Recent studies for increasing tolerance to environmental stress, through metabolic engineering of compatible solutes have shown that increased concentrations of soluble sugars and/or other osmolytes increase plant tolerance to abiotic stresses, such as drought, salinity, and cold (Rathinasabapathi 2000).
Energy and resources are required for plants to cope with abiotic and biotic stress conditions, so in sugar starvation conditions, when metabolic processes are slowed down (e.g. respiration), the plants are more sensitive to stress factors. For example, the link between low sugar content and plant sensitivity to fungal diseases known as “low-sugar diseases”, was first reported over 50 years ago by Horsfall and Dimond (1957). It must be emphasized that many environmental factors, such as insufficient light, high humidity, excessive nitrogen fertilization, and excessively deep sowing, may cause a decrease in the level of carbohydrates in host plant tissues, contributing to an increase in plant sensitivity to fungal infection (Vidhyasekaran 1974a, 1974b, Morkunas et al. 2004, Huber and Thompson 2007, Yoshida et al. 2008, Morkunas et al. 2010, Morkunas et al. 2012). By contrast, low temperature can induce plant resistance to specific pathogens, because it results in accumulation of soluble carbohydrates, affecting the cell water potential and other osmotically-active molecules, as well as accumulation of pathogenesis-related (PR) proteins (Tronsmo 1993, Thomashow 1998, Hiilovaara-Teijo et al. 1999, Płażek and Żur 2003, Yuanyuan et al. 2009). Sugar starvation of host plant cells facilitates the development of fungal pathogens because water potential is much higher there than when the concentration of soluble carbohydrates in cells is high. A lack of carbohydrates in the growth medium caused a decrease in endogenous levels of soluble carbohydrates in lupine embryo axes (Morkunas et al. 2005, Borek et al. 2006), and facilitated the development of
At some stages of plant development, sugar content may decrease considerably (so-called sugar starvation), usually under the influence of adverse environmental factors (biotic or abiotic). In this chapter, we have shown that sugar starvation in plant cells, depending on its duration, causes both ultrastructural and physiological-biochemical changes of varied severity. In non-senescent cells, the changes are aimed to maintain respiration and other basic metabolic processes at a specified level. Thus under conditions of sugar starvation, a priority is the acquisition of energy necessary for cell survival, even at the expense of organelles except the nucleus and the system supplying energy, i.e. mitochondria. The changes taking place during sugar starvation in the acclimation phase or even in the survival phase can be reversed, as long as the respiratory system functions properly. Carbon, nitrogen, and phosphorus are the major elements whose availability affects plant growth and development, so the sugar deficit signal in cooperation with nitrogen and phosphorus signaling pathways may influence plant morphology. Moreover, it is interesting that during sugar starvation, the observed processes resemble senescence. Many symptoms are identical, e.g. autophagy, decrease in protein content, and strong activation of proteolytic enzymes. However, senescence is controlled by programmed cell death. By contrast, if sugar starvation concerns non-senescent cells, then the initiated reactions cause cell acclimation to such conditions. At first these are reactions that protect cells against irreversible degradation of cell structures, especially those responsible for conservation and realization of genetic information as well as energy supply. At the second phase of sugar starvation, defense strategies are initiated, e.g. activation of the enzymatic antioxidant system, manganese ion uptake, phytoferritin accumulation, protecting cells against the destructive influence of an excess of free radicals (e.g. membrane damage). However, the mechanisms underlying the processes used by plant cells to survive sugar starvation require further research. Currently we should focus on explanation of the controlling mechanisms, which may involve signal molecules. Their synthesis may, to some extent, alleviate the influence of stress factors, and thus play an important role in plant acclimation to stress conditions. In plant cells, in response to environmental factors (either abiotic or biotic), many signaling pathways are initiated. Knowledge of the signaling pathways initiated under conditions of sugar starvation, and their cross-talk in the network, would certainly greatly help to explain the molecular mechanisms underlying plant reactions to sugar starvation.
This study was supported by the Polish Committee for Scientific Research (KBN, grant no. N N303 414437).
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