Beruflich Dokumente
Kultur Dokumente
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Guillermo Toro , and Manuel Pinto
Respiration is an oxidative process controlled by three pathways: glycolysis, the tricarboxylic acid (TCA) cycle, and
oxidative phosphorylation (OXPHOS). Respiratory metabolism is ubiquitous in all organisms, but with differences
among each other. For example in plants, because their high plasticity, respiration involves metabolic pathways with
unique characteristics. In this way, in order to avoid states of low energy availability, plants exhibit great
flexibility to bypass conventional steps of glycolysis, TCA cycle, and OXPHOS. To understand the energetic link
between these alternative pathways, it is important to know the growth, maintenance, and ion uptake components of the
respiration in plants. Changes in these components have been reported when plants are subjected to stress,
such as oxygen deficiency. This review analyzes the current knowledge on the metabolic and functional aspects of
plant respiration, its components and its response to environmental changes.
Key words: Electron transport chain, hypoxia, Krebs cycle, maintenance respiration.
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Source: Author based on Plaxton (1996) and Plaxton and Podest (2006).
Enzymes involved in each reaction are as follows: 1) sucrose synthase, 2) invertase, 3) phosphorilase, 4) and -amylase, 5) NDP kinase, 6) fructokinase,
7) hexokinase, 8) UDP-glucose pyrophosphorylase, 9) phosphoglucomutase, 10) phosphoglucose isomerase, 11) ATP-PFK, 12) PP i-PFK, 13) aldolase,
14) triose phosphate, 15) and 16) glyceraldehyde-3-phosphate phosphorylated and non-phosphorylated, respectively, 17) phosphoglycerate kinase, 18)
phosphoglyceromutase, 19) enolase, 20) PEP phosphatase, 21) H+-ATPasa, 22) piruvate kinase, and 23) H+-PPiasa.
Figure 1. Schematic representation of the glycolysis pathway and alternatives in vegetables. Continuous line represents
glycolytic flux and broken lines represent alternatives.
in Arabidopsis gin2 mutants under different lighting In turn, HXK activity in plants is related to the link
conditions. Normal growth was observed in control between glycolysis and programmed cell death
plants; however, in mutant plants (gin2/hxk1), growth (apoptosis). Briefly, mitochondrial pathways of apoptosis
was inhibited due to a reduction in cell expansion are initiated by mitochondrial cytochrome c release (high
(Moore et al., 2003). control point of apoptosis initiation) into the cytoplasm
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CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75 (Suppl. 1) AUGUST 2015
Source: Author based on Ryan et al. (2001) and Studart-Guimaraes et al. (2007).
PEP: Phosphoenolpyruvate, OAA: oxaloacetate, SSA: succinyl semialdehyde, SSADH: succinyl semialdehyde dehydrogenase, GABA: -
aminobutyric acid, GABA-T: -aminobutyric acid transaminase, GAD: glutamate decarboxylase, Glu: glucose, Ala: alanine, Pir: pyruvate.
Enzymes involved in each reaction are as follows: 1) enolase, 2) pyruvate kinase, 3) pyruvate dehydrogenase, 4) coenzyme A, 5) citrate
synthase, 6) aconitase, 7) isocitrate dehydrogenase, 8) 2-oxoglutarate dehydrogenase, 9) succinyl CoA synthase, 10) succinate dehydrogenase, 11)
fumarase, 12) malate dehydrogenase, 13) phosphoenolpyruvate carboxylase, 14) isocitrate lyase, 15) malate synthase.
Figure 2. Schematic representation of tricarboxylic acid cycle (TCA) in plants. Red line: TCA cycle, green line: glyoxylate cycle, gray line:
GABA route.
metabolite in plants with an unclear function; however, stress responses (Kinnersley and Turano, 2000). Unlike in
at present there is evidence to indicate that GABA plants, in mammals GABA clearly functions as a
plays a major role in C metabolism in response to stress molecular neurotransmitter in the brain (Bouch and
(Bouch and Fromm, 2004). As shown in Figure 2, the Fromm, 2004).
GABA pathway is composed of three enzymes; glutamate The glyoxylate cycle is another pathway associated
decarboxylase (GAD), a cytoplasmic enzyme, and two with the TCA cycle in plants, defined as a
mitochondrial enzymes called GABA transaminase and modification of the TCA cycle (Figure 2) (Kornberg and
succinic-semialdehyde dehydrogenase (GABA-T and Madsen, 1958). In turn, it has mainly been associated
SSADH, respectively), present both in animals and plants with lipid metabolism in seeds of oil plants (Eastmond
(Bouch and Fromm, 2004; Sweetlove et al., 2010). In and Graham, 2001). In general, the difference between
plants, it has been observed that GABA pathway glyoxylate cycle and TCA cycle is that the first
responds quickly to environmental changes, e.g. it is avoids two points of decarboxylation and allows the
stimulated under conditions of cold, salinity (Kinnersley generation of acetyl CoA through - oxidation of fatty
and Turano, 2000), and anoxia (Aurisano et al., 1995). The acids, giving rise to succinate, which is then
role of GABA pathway in plants is still unclear because incorporated into the mitochondria to generate OAA,
studies on this pathway are relatively new. However, it which will go directly toward the synthesis of sucrose by
could be that GABA pathway is linked to many abiotic gluconeogenesis (Eastmond and Graham, 2001).
Source: Author based on Peltier and Cournac (2002) and Bauwe et al. (2010).
i e
OXPHOS abbreviations: I: cytochrome I or NADH dehydrogenase, ND2 , ND2 , NAD(P)H dehydrogenase type II internal and1 external, respectively, II:
cytochrome II or succinate dehydrogenase, UQ: ubiquinone, AOX:i alternative oxidase; III: cytochrome c reductase or cytochrome bc , IV: cytochrome c oxidase
or COX, ATPase: ATP synthase, U or UCP: uncoupling protein, PP asa: pyrophosphate synthase.
Chlororespiration abbreviations: OAA: oxaloacetate, PSII: photosystem II, PQ pool of plastoquinone, Ndh or NAD(P)H-PQ, NAD(P)H
dehydrogenase complex or NAD(P)H-plastoquinone oxidoreductase, respectively, Cyt b6/f, cytochrome b6/f, PC: plastocyanin, PSI: photosystem I,
Fd: ferredoxin, FNR: ferredoxin NADP + reductase.
Figure 3. Schematic representation of oxidative phosphorylation (OXPHOS) (A) and chlororespiration (B).
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the inner mitochondrial membrane is the force that OXOPHOS control points (Lambers, 1982). Studies
drives ATP synthesis (Millar et al., 2011). have elucidated a crucial role of AOX in protecting against
In plants, studies have focused on finding ROS produced during oxidative stress (van Dongen et al.,
alternative pathways to the conventional OXPHOS 2011), and it can also influence mitochondrial
pathway of the electron transport chain. For example, the adaptability to different kinds of stress (Moller, 2001;
participation of certain alternative pathways that involve Rasmusson et al., 2009), even expressing mitochondrial
proteins associated with complex I (Rasmusson et al., 2004) genes in a wide variety of environments. AOX acts against
and AOX (Moore et al., 2002) has been proposed (Figure ROS as follows: AOX allows electron transfer from
3). However, non-phosphorylation pathways do not ubiquinone (UQ) to O2, which high levels of reducing
contribute to the generation of the inner-membrane proton agents in the UQ pool can be dissipated through AOX, thus
gradient (Fernie et al., 2004). To overcome this
avoiding the formation of ROS (Polidoros et al., 2009).
deficiency in the proton gradient, plants have a strategy
developed from uncoupling proteins (UCP) embedded in Chlororespiration
the inner mitochondrial membrane (Smith et al., 2004; In plants, it is possible for electron transport to O 2 to occur
Arnholdt-Schmitt et al., 2006). Uncoupling proteins activity in the presence of light through thylakoidal membranes of
can enhance the transfer of protons into the mitochondria by chloroplasts, via chlororespiration (Figure 3) (Polidoros et
controlling the rate of production of superoxides, and may al., 2009), distinct from photorespiration (Bennoun,
even have some control over the TCA cycle, because 1982; Peltier and Cournac, 2002) and the Mehler reaction.
increases in the UCP content can increase the rate of The function of this process is to ensure supplies of ATP and
conversion of pyruvate to citrate (Smith et al., 2004). NAD(P)H generated by glycolysis for converting starch into
In both plants and animals, once in the mitochondria, triose phosphate (D-glyceraldehyde phosphate or
NADH and FADH2 are oxidized in a complex called dihydroxyacetone phosphate) (Bauwe et al., 2010;
NADH dehydrogenase or complex I (Figure 3A), which Maurino and Peterhansel, 2010). Both chloroplasts
initiates the transfer of electrons through OXPHOS. In and mitochondria share similar mechanisms and control
plants this complex has 46 subunits, of which only 32 components, e.g. the electron transport is carried out in the
are similar to complex I proteins present in animals membrane and shares the same membrane components
(Millar et al., 2011). A study in Arabidopsis showed that (cytochrome, ion-S proteins, quinones and ATPase)
plants without complex I could still survive in (Bennoun, 1982). Although there are no exclusive carriers
association with a complex I protein called NAD(P)H of NAD(P)H in the thylakoidal membrane, this may be
dehydrogenase (Fernie et al., 2004) . According to their performed indirectly through OAA-malate ports which allow
position on the inner mitochondrial membrane, there are the transport of malate (Figure 3), being oxidized by
two kinds of NADPH dehydrogenase, internal and NAD+ to produce NADH in the chloroplast stroma
external (ND2i and ND2e, respectively) (Rasmusson et (Bennoun, 1982). The ability to transport reducing
al., 2004). The function of ND2 e is related to the agents through the inner chloroplast membrane means that
regulation of NADH and NAD(P)H reduced in the it is in communication with the rest of the cell. There have
cytoplasm in response primarily to the cytoplasmic Ca been studies on the importance of environmental changes in
concentration, while ND2i participates with substrates chlororespiration, with an increase in the activity and
from the TCA cycle (Rasmusson et al., 2004). expression of a protein complex called NDH (homologous
Complex II (succinate dehydrogenase, SDH) is an to complex I) (Peltier and Cournac, 2002). This complex
enzyme shared between TCA cycle and OXPHOS catalyzes the transfer of electrons from NAD(P)H to
(Figure 2 and 3). Succinate dehydrogenase has different plastoquinones (Rumeau et al., 2005). According to some
functions depending on the tissue in which it is found. authors, this complex is key in chlororespiration because it
For example, some influence of SDH has been has an NADH dehydrogenase function in mitochondria. In
reported in leaves with phytochrome A, which controls turn, the Ndh complex regulates the proton gradient
the activity of SDH (Plaxton and Podest, 2006). produced in the stroma, suggesting a role in the control of
Complexes III and IV (cytochrome c reductase and oxidative stress produced in the chloroplast stroma
cytochrome c oxidase (COX), respectively) correspond (Rumeau et al., 2005).
to the OXPHOS supercomplex, COX being a prime
OXOPHOS terminal oxidase (Popov et al., 2010). Photorespiration
Despite COX, there is another terminal oxidase that is Unlike chlororespiration, photorespiration (also called the
inserted in the inner mitochondrial membrane, called C2 cycle) corresponds to an oxidation mechanism of C
alternative oxidase (AOX) (Figure 3). Is was thought that molecules (such as ribulose 1,5-diphosphate) and is
AOXs function was to support the transfer of electrons performed in three different organelles: chloroplasts,
when COX was at full capacity (van Dongen et al., 2011). mitochondria and peroxisomes (Peltier and Cournac, 2002).
Nevertheless, is known that both AOX and COX compete This process consists in replacing CO 2 for O2 during C
for electrons, because both are positioned at critical fixation in photosynthesis, allowing recycling
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and transforming the phosphoglycolate (2PG) generated protein turnover (Poorter et al., 1991), maintenance of
into phosphoglycerate (Maurino and Peterhansel, 2010). protons gradient (De Visser et al., 1992; Bouma et al.,
Photorespiration is one of the most important pathways 1994; Scheurwater et al., 2000), waste mechanisms and
of carbon metabolism in plants, exceeded in its importance heat production by alternative pathways (Veen, 1980;
at the terrestrial level only by photosynthesis. This is Bouma and De Visser, 1993). Generally, these processes
because of the high O2 concentration in the cells compared are associated with two components of respiration: growth
to CO2. Photorespiration can release about 20% of the CO 2 and maintenance respiration (Johnson et al., 1998).
that is absorbed during photosynthesis under normal Nevertheless, it is possible aggregate a third component
temperatures. However, it was determined that the amount when the correlation between relative growth rate (RGR)
of CO2 released could be higher in hot and dry and net N uptake rate (NNUR) is not tight (Amthor, 2000;
environments (Bauwe et al., 2010; Maurino and Thornley and Cannell, 2000).
Peterhansel, 2010). The interaction between Growth respiration is respiration that produces energy
photorespiration and mitochondrial respiration is generated and C skeletons for the synthesis of new structures
from an allosteric reaction in the TCA cycle using the in growing plants (proteins, lipids, organic acids, and
products of the reaction catalyzed by glycine
structural carbohydrates) (Veen, 1980). Maintenance
decarboxylase (GDC) and an interaction between NAD + respiration is respiration that produces energy for all
regenerated by the GDC and the electron transport chain processes related to cellular maintenance such as protein
(Figure 3B). turnover, maintenance of ion gradients and membrane
The importance of photosynthesis and photorespiration potentials in the cell (Penning de Vries et al., 1974;
has been observed in tobacco (Nicotiana tabacum Penning de Vries, 1975). A mathematical expression of
L.) mutants deficient in complex I expression for the relationship between these components of respiration
mitochondrial OXPHOS, because the proteins of complex I is: [1]
are important for maintaining the redox conditions in the Rr = Rm + cg RGR + cu NNUR
cell that enhance photosynthetic efficiency (Peltier and where Rr is root respiration rate (mol O2 or CO2 g-1 d-1), Rm
Cournac, 2002; Plaxton and Podest, 2006; van Dongen is respiration rate to produce ATP required for maintenance
et al., 2011). of biomass, cg is root respiration to produce ATP for
cellular compound synthesis (mmols O2 or CO2 g-1), RGR
Functions of plant respiration is the relative growth rate of roots (mg g -1 d-1), cu is the
There is a great deal of information available about respiration rate required for maintenance (mol g -1
molecular and physiological aspects of plant respiration and d-1), and NNUR is the net N uptake rate (Veen, 1980).
its importance for plant growth and development. However, The energy requirements for each process depend on
there is little information about the link between respiration the rates associated with them, which are affected by the
and key processes in the survival of several plant species. species, organ (tissue) and environmental conditions to
Nine processes have been described to take priority from which the plants are subjected (Lambers, 2008).
the energetic point of view: growth (Dutilleul et al., 2003), For example, Figure 4 shows that young plants under
nitrate reduction, symbiotic N fixation, uptake of nitrate high N conditions allocated only 10% to the maintenance
and other ions by roots (van Iersel and Seymour, component of root respiration (Poorter et al., 1991). On
2000; Thongo MBou et al., 2010), the other hand, the growth component is an important
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CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75 (Suppl. 1) AUGUST 2015
part of root respiration (20%-45%); however, the values
-1
of 1.2 to 1.4 g glucose g -1 DM (0.2 to 0.4 g CO 2
majority of the respiration is devoted to the ion uptake g DM) (Cannell and Thornley, 2000).
process (50%-70%) (Poorter et al., 1991). In a study in Currently, other studies focus on the contributions that
Carex, maintenance respiration was the most important terminal oxidases (COX and AOX) should have on the
component associated with respiration because fully growth and maintenance components of plant respiration. In
grown plants were used, which meant lower RGR and Arabidopsis plants, Cannell and Thornley (2000) estimated
NNUR (van der Werf et al., 1988). the construction cost of leaf tissues, which corresponded to
Protein turnover corresponds to the major fraction of the 5.3 and 0.8 mmol O2 g- 1 DM for COX and AOX,
maintenance component of respiration. It is particularly respectively, while maintenance respiration via COX and
important when rapid changes occur in the environment or AOX was 14.3 and 9 nmol O 2 g-1 s-1. Similar values were
during periods of stress. Without this mechanism (protein found by Florez-Sarasa et al. (2007) in the same species.
turnover), the energy requirement would be increased by a Respiration through COX consumed 90% and 60% of
high demand from the plant, so protein turnover could keeps respired C for growth and maintenance, respectively, while
the metabolism stable in a wide variety of environments and AOX consumed 10% and 40% of available C for growth
at all stages of development (van der Werf et al., 1988). It is and maintenance respiration, respectively (Bouma,
estimated that between 2% and 5% of all proteins are 2005). These results show an interesting effect, because
replaced daily; however, there are reports indicating that respiration through
protein turnover in leaves could be as much as 20% daily. COX varies more in response to RGR than AOX (Florez-
Some of the processes associated with protein turnover are: Sarasa et al., 2007). When RGR is low (decreasing or
biodegradation of proteins, activation and turnover of amino not the respiration) AOX activity is increased, allowing
acids, peptide bond formation and posttranslational it to maintain the redox state of the ubiquinone pool to
processes, among others (Bouma et al., 1994). inhibit ROS (Florez-Sarasa et al., 2007).
Some researchers working under different growth Oxygen availability for plant respiration
conditions, have correlated maintenance respiration rates A major factor that affects plant respiration is O 2 depletion, in
and protein content of biomass (Poorter et al., 1991); thus, it the rhizosphere or directly in tissues. The O2 availability in
can be inferred that protein turnover costs are the most tissues and cells depends on the plants age and especially on
important costs of maintenance respiration. In a comparative the O2 supply from the environment, tissue O 2 having a great
study on roots of fast-growing (Dactylis glomerata L.) and influence on the central pathways of carbohydrate synthesis
slow-growing (Festuca ovina L.), it was shown that the (Millar et al., 1998). In plants, the major external factors
cost associated with protein turnover accounted for between affecting O2 availability are flooding and waterlogging of soil
22% and 33% of daily ATP production, corresponding to (Liao and Lin, 2001).
11% to 15% of the total production of ATP by roots Under these conditions we can distinguish three broad
(Hachiya et al., 2007). In leaves, protein turnover has been categories of oxygen status induced by water: normoxia,
estimated at approximately 200 mmol CO2 kg-1 d-1 hypoxia, and anoxia (Table 1). Excess water in soil
(Scheurwater et al., 2000). Another portion of the costs decreases the O2 diffusion rate, because the diffusion of
associated with maintenance are dedicated to regulating the O2 is 10 4 times slower in water than in air (Liao and
ionic gradient, also known as the cells osmotic potential, Lin, 2001; Jackson and Colmer, 2005). The reason
where the costs of maintaining the ionic gradient are for this is the high level of interaction between O 2 and
approximately 400 mmol CO2 kg-1 d-1 (Amthor, 2000). H2O through hydrogen bonds (Mommer et al., 2004).
Otherwise, the growth component is usually expressed in In flooded soils not only is the diffusion of O2 reduced,
C units (cg from Equation [1]), corresponding to new but also the diffusion of several other gases such as CO 2 and
biomass per unit of glucose (Penning de Vries, 1975). Most ethylene (Wegner, 2010). It is important to consider that low
plant cg values are between 0.7 and 0.8, equivalent to the O2 availability in cells can even occur in some situations
cost of constructing the glucose requirement, with under normoxia, due mainly to a high resistance
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to O2 diffusion between different plant tissues (Gibbs the availability of O2 in roots is decreased, adaptation to
and Greenway, 2003) such as roots and stems (van stress may occur through two strategies; the first is a
Dongen et al., 2011). decrease in ATP consumption which leads to a metabolic
Sometimes, to reduce the anaerobic state in shoots, roots crisis at the cellular level (Igamberdiev et al., 2010), and the
regulate frequency of absorption (Armstrong et al., 1994; second is an increase in the glycolytic flux (Mancuso
Zabalza et al., 2009) and oxygen consumption and Marras, 2006). The latter is called the Pasteur effect
(Mancuso and Marras, 2006). Morphological adaptations (Gibbs et al., 2000), consisting of a progressive acceleration
also play a key supporting role in promoting the O 2 flux in carbohydrate metabolism that allows the plants to
from the roots through the rest of the plant, e.g. maintain their energy level, especially during the early
aerenchyma formation due to induction by ethylene phase of acclimation to oxygen deficiency (Turner,
(Greenway and Gibbs, 2003). One of the main effects of 1951; Greenway and Gibbs, 2003; Camacho-Pereira et
anaerobiosis on metabolism is a decreased adenylate al., 2009; Wegner, 2010).
energy charge (AEC), which also reduces the ATP:ADP Although many authors emphasize the importance
ratio (Drew et al., 2000). of the Pasteur effect in acclimatization processes to
Under hypoxic conditions the TCA cycle pathway gives compensate for the energy inefficiency caused by
more flexibility to the overall metabolism (Table 1). OXPHOS inhibition (Gibbs and Greenway, 2003; Huang
For instance, in Lotus japonicus, it was shown that alanine et al., 2008), this can only generate ATP at about 37.5%
aminotransferase (AlaAT) generates a link between of the rate produced in tissues under optimal oxygen
glycolysis and the TCA cycle through the conversion of 2- conditions (Geigenberger, 2003).
oxoglutarate to succinate. This generates NADH that is used The O2 is a molecule that participates as a final
in the transformation of OAA into malate; together with electron acceptor in the transport chain complexes (Gibbs
succinate CoA ligase, both contribute to the generation of and Greenway, 2003); therefore, when oxygen availability
ATP under conditions of oxygen deficit (Geigenberger, decreases dramatically in the rhizosphere
2003; Bailey-Serres and Voesenek, 2008). (anoxia, Table 1), OXPHOS is inactivated (Moller, 2001)
Moreover, glycolysis is affected when O 2 concentration and terminal oxidase (COX) is inhibited (Liao and Lin,
falls below 1.5-2.0 mg O2 L -1 in the bulk solution 2001; Greenway and Gibbs, 2003; Mancuso and Marras,
(hypoxia). This decreases glycolysis and increases the 2006; Mailloux et al., 2007). Under these conditions,
plants have developed alternative pathways to aerobic
activities of enzymes involved in fermentation (Li et al.,
respiration in order to maintain glycolysis through the
2010). In maize subjected to hypoxia, PDC activity
increases 5-to-9-fold compared to that under normal regeneration of NAD+ (Gupta et al., 2009) and thus
conditions (Gupta et al., 2009). It is known that there are obtain the energy needed to maintain key processes of
two major control points for electron transfer under oxygen metabolism such as membrane integrity and thus ion
selectivity (Tadege et al., 1999), protein synthesis and
deficit, corresponding to AOX and COX. Some studies
turnover and regulation of cytosolic pH, among others
suggest that the response to oxygen deficiency in roots
(Blokhina et al., 2003). These alternative pathways
is driven by the terminal oxidation of respiration (Kennedy
et al., 1992). Under some conditions, when are known as fermentations.
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CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75 (Suppl. 1) AUGUST 2015
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