Experimental Plant Biology: Why Not?!
Involvement of mitochondria in the control
of plant cell NAD(P)H reduction levels
Allan G. Rasmusson1 and Sabá V. Wallström
Department of Cell and Organism Biology, Lund University, Sölvegatan 35B, SE-223 62 Lund, Sweden
Abstract
NADPH and NADH mediate reductant flow between cellular processes, linking central carbon and energy
metabolism with intermediary metabolism, stress defence and development. Recent investigations have
revealed paths of functional interactions, and have suggested that mitochondrial NADPH oxidation, especially
together with the oxidative pentose phosphate pathway, is an important regulator of the cytosolic NADPH
reduction level. Furthermore, stress-dependent metabolic pathways substantially affect the NADPH reduction
level in particular physiological situations. The mitochondrial impact on the NADPH reduction level provides
a model example of the physiological significance of the mitochondrial NAD(P)H dehydrogenase set-up,
which is more complex in plants than in other organisms.
Introduction
Oxidation of NAD(P)H by the mETC
The pyridine nucleotides NAD(H) and NADP(H) are central
mediators of reductant energy between metabolic processes in
cells. Traditionally, NADH has been associated with catabolic
processes such as respiration and NADPH with anabolic processes such as photosynthesis. However, the distinction has
been shown to be less clear. In plants, for example, NADH
also functions in plastids and NADPH in mitochondria [1,2].
In later years, investigations in mammals have shown that the
pyridine nucleotides exert many cellular effects and signalling
functions. Apart from their roles in energy metabolism and
thiol-reductant maintenance, pyridine nucleotides have been
associated with Ca2+ homoeostasis and gene regulation, cell
death, aging, oxygen sensing and exocytotic insulin release
[3–6]. Signalling functions of pyridine nucleotides have also
been described in plants [7,8].
The metabolism in plants deviates from that in mammals
by its multitude of biochemical pathways that function
under different developmental and environmental conditions.
Among the major differences is the highly complex
mETC (mitochondrial electron-transport chain), which, in
particular, contains a system of alternative pathways –
type II NAD(P)H dehydrogenases and AOXs (alternative
oxidases) – that allow a larger flexibility in the oxidation
of NAD(P)H in plants. The present review focuses on the
recent developments in the field of mitochondrial NAD(P)H
oxidation and how changes in the oxidation may modulate
cellular NAD(P)H reduction levels and associated biological
processes.
Plant type II NAD(P)H dehydrogenases and AOXs
(Figure 1) are energy bypasses around the large multiprotein
complexes of oxidative phosphorylation. Type II NAD(P)H
dehydrogenases reduce ubiquinone and thus circumvent
respiratory complex I, whereas AOX bypasses complexes
III and IV of the cytochrome pathway by directly oxidizing
ubiquinol [9–12]. Respiration via the proton-pumping
complexes I, III and IV creates a proton gradient that is used
by the ATP synthase for ATP production. Type II NAD(P)H
dehydrogenases and AOXs do not pump protons. Therefore
the activity of these proteins leads to a lower ATP production
and thus decreases the respiratory energy conservation. In
addition, plant mitochondria contain a family of uncoupling
proteins that allow a direct proton influx across the inner
mitochondrial membrane and therefore directly bypass the
ATP synthase [13].
The model plant Arabidopsis contains five AOX
genes, AOX1a–AOX1d and AOX2 [14], but functional
differences between homologues are not known. Mitochondrial type II NAD(P)H dehydrogenases are encoded by three small gene families. In Arabidopsis, there are
seven genes called AtNDA1, AtNDA2, AtNDB1–AtNDB4
and AtNDC1 [15]. For all genes, encoded proteins have been
localized to mitochondria [15–17]. Within mitochondria,
the NDA1 protein in both Arabidopsis and potato is
most likely to be an internal matrix-oriented NADH
dehydrogenase and an internal location was also shown
for AtNDA2. AtNDC1 has likewise been located to the
matrix surface of the inner membrane, whereas the NDB
proteins analysed in potato and Arabidopsis are external
[15,17–20]. NDB1 in both potato and Arabidopsis is an
external Ca2+ -dependent NADPH dehydrogenase [20,21].
The AtNDB2 and AtNDB4 proteins are Ca2+ -stimulated and
Ca2+ -independent NADH dehydrogenases respectively [21].
Although all the plant type II NAD(P)H dehydrogenases
investigated appear to reside in mitochondria, functions also
Key words: carbon metabolism, mitochondrial electron transport, NAD(P)H, redox homoeostasis,
stress.
Abbreviations used: AOX, alternative oxidase; GFP, green fluorescent protein; mETC,
mitochondrial electron-transport chain; OPP, oxidative pentose phosphate pathway.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2010) 38, 661–666; doi:10.1042/BST0380661
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Figure 1 Standard and alternative enzymes in the mETC in plants
The standard complexes are depicted in white, including the proton-pumping complexes I, III and IV. Type II NAD(P)H
dehydrogenases and AOX are depicted in grey shading. Broken lines denote presently unclear enzymatic properties. SDH,
succinate dehydrogenase.
in other parts of the cell cannot be ruled out. A type II
NADPH dehydrogenase in Chlamydomonas functions in
chloroplast electron transport [22]. In Arabidopsis, NDC1
has been detected in plastoglobules in chloroplasts [23–25].
A dual location of NDC1 in mitochondria and chloroplasts
has been supported by targeting analyses using GFP (green
fluorescent protein) [16]. In the same investigation, C-termini
of NDA1, NDA2 and NDB1 targeted GFP to peroxisomes,
whereas whole reading frame constructs with C-terminal
GFP specified targeting to mitochondria. Western blotting
signals, using antibodies against NDA proteins, have been
observed in potato and Arabidopsis peroxisomes [16,26].
However, in potato, a weak interaction with the most
abundant peroxisomal protein, catalase, which has a similar
molecular mass to that of NDA proteins, could not be ruled
out [26]. Potato NDB1 was not detected in peroxisomes
[26,27]. It is presently unclear whether the peroxisomal
targeting peptides are functional in the native NDA1, NDA2
and NDB1 proteins. Further investigations are also needed
for determining putative functions of type II NAD(P)H
dehydrogenases in organelles other than mitochondria,
and whether this would constitute an appreciable flux of
NAD(P)H oxidation.
Redox level specificity of the cytosolic and
mitochondrial NAD(P)H pools
The presence of type II NAD(P)H dehydrogenases with
different properties on both sides of the mitochondrial inner
membrane, allows the mETC to specifically regulate the
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Authors Journal compilation reduction levels of either mitochondrial or cytosolic NADH
or NADPH. For cytosolic NAD(P)H, this may be regulated
by cytosolic Ca2+ , which activates the external NADH
dehydrogenase NDB2 and the NADPH dehydrogenase
NDB1 [9,21]. By differential regulation, the setup of type II
NAD(P)H dehydrogenases allows specific modulations of
distinct cellular redox pools. In comparison, changes in
activity of AOX alone should simultaneously affect both
matrix and cytosolic pools of NADH and NADPH. Changes
in uncoupling protein activity should likewise modify the rate
of oxidation for several mETC substrates due to an increase in
ubiquinol oxidation in the presence of a lower electrochemical
proton gradient across the inner mitochondrial membrane.
However, in combination, an increase in the enzymatic
capacity of an NAD(P)H dehydrogenase can direct an
increased rate in AOX or uncoupling protein to make the
mETC preferentially utilize a particular reductant source, and
at an elevated flux. In line with such a view, genes encoding
type II NADH dehydrogenases and AOXs have been
demonstrated to be pairwise co-expressed upon comparisons
of microarray data for stress and developmental series [28–
30]. An example where a need for compartment specificity of
NADH oxidation is anticipated relates to the light induction
of the internal enzyme NDA1 in potato and Arabidopsis
[15,31]. This induction suggests that the enzyme is active
in stabilizing the matrix NADH reduction level during
photorespiration, when a massive production of NADH
occurs in the mitochondrial matrix [11,32].
Of central importance for a redox separation between
compartments are the major citric acid cycle enzymes and
Experimental Plant Biology: Why Not?!
Figure 2 Summary of paths for electrons and regulatory effects relating to the NAD(P)H homoeostasis in plants
NDex and NDin are external and internal type II NAD(P)H dehydrogenases respectively. GHB, γ -hydroxybutyrate;
UQ, ubiquinone.
the metabolite exchangers that together mediate reductant
shuttling across the inner mitochondrial membrane. The
reduction levels of NADH in the matrix and the cytosol are
believed to equilibrate primarily with the malate/oxaloacetate
ratios in each compartment (with secondary equilibration to
the molecules of the glutamate:oxaloacetate transamination
reaction). An exchange of malate and oxaloacetate can then
communicate reductant from the mitochondrion to the
cytosol, yet maintaining a sharp gradient of the NADH
reduction level from the matrix to the cytosol [33–36]. In
vivo evidence for NADH-mediated mitochondrially induced
whole-cell redox changes has especially been obtained with
the CMSII (cytoplasmic male sterile II) mutant, deficient
in mitochondrial complex I, as reviewed previously [36,37].
However, similar investigations for the type II NADH
dehydrogenases have not been carried out.
Regarding the NADPH reduction, relatively less is
known. In contrast with NAD(H), NADPH reduction
levels were not in equilibrium with the major organic
acid couples in spinach leaves [34]. Determinations of
subcellular concentrations in pea leaf protoplasts revealed
that the mitochondrial NADPH reduction level was highly
variable with light and carbon dioxide supply, whereas the
cytosolic levels were constant [38]. This demonstrated that
a variable gradient of reduction level exists between the
matrix and cytosolic NADPH pools, and it was suggested
that the mitochondrion can export reductant to the cytosol
as NADPH by a citrate valve, exchanging citrate and 2oxoglutarate [38].
Regulation of the cytosolic NADPH
reduction level
The major carbon pathways that can maintain the cytosolic
NADPH reduction level by NADP+ reduction are the OPP
(oxidative pentose phosphate pathway) [39], the cytosolic
NADP–isocitrate dehydrogenase that produces 2-oxoglutarate for nitrogen assimilation using carbon derived
from mitochondrial citrate [40], a triose-phosphate shuttle
suggested to export reductant from the chloroplast in the
light [41] and the citrate valve that would export reductant
from mitochondria under photorespiratory conditions [38]
(Figure 2). Additionally, NADP(H) can be synthesized as
NADP or NADPH by the non-redox reactions of cytosolic
NAD(H) kinases [42]. NADPH is utilized as a reductant
by several vital processes. The thiol-reducing enzymes,
such as glutathione reductase and thioredoxin reductase,
mediate thiol group-based regulatory and antioxidative
cellular functions [43,44]. The NADPH oxidase of the plasma
membrane mediates pathogen responses and signalling
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during stress and development [45]. Alternatively, the external NADPH dehydrogenase NDB1 of the mETC can oxidize
NADPH using oxygen as the terminal acceptor [20]. In
addition, a large range of biosynthetic pathways utilize
NADP(H) in reductive and oxidative steps. As several of the
NADPH-associated processes are assumed to be controlled
by the demands of the products, major candidates for taking
part in the control and regulation of the NADPH redox level
are the NADP+ -reducing pathways and the mitochondrial
external NADPH dehydrogenase.
Several of the NADPH-associated pathways mentioned
above are mainly active in the light, including the triosephosphate shuttle, the suggested citrate valve and, at least
under nitrate nutrition, the NADP–isocitrate dehydrogenase.
They are likely to contribute significantly to the NADP+
reduction under high light or photorespiratory conditions,
but by their dependence on external factors, they are less
likely to mediate basal control of the NADPH reduction
level, especially in non-green organs. In an Arabidopsis
mutant lacking the cytosolic NADP–glyceraldehyde-3phosphate dehydrogenase (the NADPH-generating enzyme
of the triose-phosphate shuttle), a surprising increase in
NADPH reduction levels was observed in leaves [46].
It was suggested that an increase observed in OPP
glucose-6-phosphate dehydrogenase expression may have
induced an over-compensation, indicating that this enzyme
has a stabilizing effect on NADPH levels. Glucose-6phosphate dehydrogenase has several isoenzymes that have
different localizations in the cytosol and in plastids and
are characterized by variations in sensitivity to NADP+
and NADPH [47]. Treatment of tobacco cells with the
elicitor cryptogein leads to an NADPH oxidase burst, which
decreases the cellular NADPH reduction level, but is again
compensated for by an increased OPP activity [48]. Recently,
it was shown further that replacement of the cytosolic
glucose-6-phosphate dehydrogenase for a less NADPHinhibited plastidic isoform in tobacco increased the NADPH
oxidase-mediated oxidative burst and stress tolerance [49].
It is therefore evident that the OPP has an important role
in maintaining NADPH reduction, and it is likely that
variations in the cytosolic NADPH reduction level will affect
the capacity for defence against plant stress.
Recently, it was shown that the cellular NADPH reduction
level can be modulated by the mitochondrial NADPH
oxidation. Transgenic Nicotiana sylvestris with increased
levels of the external NADPH dehydrogenase NDB1
from potato displayed decreased NADPH reduction in
leaves in moderate light, but not in high light [27,50].
The decreased NADPH in moderate light did not lead
to changes in chloroplast redox markers, indicating that
export of reductant from the plastid is governed by the
intrachloroplastic redox status, rather than the cytosolic.
In the stem apex, where most cells are non-photosynthetic,
the overexpression or suppression of NDB1 substantially
affected the cellular NADPH reduction level. Furthermore,
the stem NADPH/NADP+ ratio negatively correlated
with the expression of floral meristem identity genes, and, as
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Authors Journal compilation Figure 3 Putative modes of influence of the NDB1 enzyme and
the NADPH reduction level on stem bolting
The decreased NADPH/NADP+ ratio may either be sensed directly by
an NADP(H)-binding protein, or be mediated by secondary changes in
metabolites (e.g. sugars).
a consequence, also with stem bolting (Figure 3). The effect
was possibly mediated by the observed NADPH-associated
changes in sugar metabolism [27]. A strong decrease in
NADPH reduction was seen during stem bolting [27],
which may function by increasing the supply of NADP+
to oxidative biosynthetic processes. This association of a
lowered NADPH reduction level with stem elongation
stands in contrast with the need for a high NADPH
supply in plant defence reactions [49], indicating that
cytosolic NADPH reduction may balance reciprocal cellular
functions. Recently, it was also shown that abiotic stresses
(cold, heat and submergence) are associated with increased
NADPH reduction levels, driven by NADP+ -reducing γ hydroxybutyrate formation via the γ -aminobutyrate shunt
[51]. In this case, the glutamate precursor of the γ aminobutyrate shunt varied inversely with the NADPH
reduction, whereas in non-stressed growing heterotrophic
tissues, a positive connection between OPP or NADPH
reduction level and the 2-oxoglutarate to glutamate reaction
has been observed [27,52,53]. This illustrates that the control
of the NADPH reduction level, and the NADPH influence
on carbon metabolism varies in mode between different
organs and physiological situations.
A major crossover point in the NADPH homoeostasis is
the stress-imposed cytosolic Ca2+ influx. Elevated Ca2+ levels
activate the NADPH oxidase [48,54,55], the mitochondrial
NADPH oxidation [21], the γ -aminobutyrate shunt [56]
and NAD(H) kinases [7]. Especially, the mitochondrial
NADPH oxidation may be in competition with the NADPH
oxidase function. For further understanding of the
NADPH reduction level regulation, it is therefore important
that more exact information becomes available on how Ca2+
signalling may segregate between the different NADP(H)utilizing pathways.
Experimental Plant Biology: Why Not?!
Conclusions
Plant mitochondria contain a uniquely complex set-up of
NAD(P)H dehydrogenases, the details and physiological importance of which are becoming revealed, especially regarding
the oxidation of cytosolic NADPH. The NADPH reduction
level control is distributed over several metabolic processes,
and varies depending on organ identity and environmental conditions. In particular, the distribution of control
is anticipated to depend on the activity of light-dependent
redox shuttles, stress-associated redox-dependent production
of defence molecules, and growth-dependent demands for
NADP+ and NADPH. A basic control by reduction via the
OPP and oxidation via the external mitochondrial NADPH
dehydrogenase is, however, expected to be relevant in a
majority of metabolic situations.
Funding
We acknowledge financial support from The Swedish Research
Council.
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Received 13 October 2009
doi:10.1042/BST0380661