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10.1146/annurev.arplant.55.031903.141720
Annu. Rev. Plant Biol. 2004. 55:23–39
doi: 10.1146/annurev.arplant.55.031903.141720
c 2004 by Annual Reviews. All rights reserved
Copyright First published online as a Review in Advance on February 25, 2004
Annu. Rev. Plant Biol. 2004.55:23-39. Downloaded from arjournals.annualreviews.org
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ALTERNATIVE NAD(P)H DEHYDROGENASES
OF PLANT MITOCHONDRIA
Allan G. Rasmusson,1 Kathleen L. Soole,2
and Thomas E. Elthon3
1
Department of Cell and Organism Biology, Lund University, SE-223 62 Lund, Sweden;
email: [email protected]
2
School of Biological Sciences, Flinders University, Adelaide, South Australia 5001,
Australia; email: [email protected]
3
School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588;
email: [email protected]
Key Words NADH, dehydrogenases, internal, external
■ Abstract Plant mitochondria have a highly branched electron transport chain that
provides great flexibility for oxidation of cytosolic and matrix NAD(P)H. In addition to
the universal electron transport chain found in many organisms, plants have alternative
NAD(P)H dehydrogenases in the first part of the chain and a second oxidase, the
alternative oxidase, in the latter part. The alternative activities are nonproton pumping
and allow for NAD(P)H oxidation with varying levels of energy conservation. This
provides a mechanism for plants to, for example, remove excess reducing power and
balance the redox poise of the cell. This review presents our current understanding of
the alternative NAD(P)H dehydrogenases present in plant mitochondria.
CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
NAD(P)H DEHYDROGENASE ACTIVITIES IN INTACT
MITOCHONDRIA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
External NAD(P)H Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Internal NAD(P)H Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
EFFORTS TO PURIFY ALTERNATIVE NAD(P)H
DEHYDROGENASES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
PLANT HOMOLOGS OF BACTERIAL AND FUNGAL
NAD(P)H DEHYDROGENASES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
PHYSIOLOGICAL ROLES OF ALTERNATIVE NAD(P)H
DEHYDROGENASES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CONCLUDING REMARKS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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INTRODUCTION
Biochemical investigations of isolated plant mitochondria have indicated that they
are unique in many respects, including their ability to oxidize NADH and NADPH
via several dehydrogenases (5, 23, 30, 61, 64, 68, 92). To understand NAD(P)H
oxidation in plant mitochondria, knowledge of mitochondrial structure and compartmentalization is essential. Mitochondria have two membrane systems that functionally delineate them into four regions (Figure 1). The outer membrane (OM)
contains relatively few proteins, and is not osmotically active. A prevalent OM
protein, porin, allows free passage of most small molecules, including NAD(P)H,
through its pore. In contrast, the inner mitochondrial membrane (IM) is osmotically
active and impermeable to most solutes. It contains numerous proteins including
specific transporters for substrates, ions, and macromolecules as well as most components of the electron transport chain. The space between the IM and OM, the
intermembrane space, contains relatively few but essential proteins. For example,
cytochrome c is a soluble protein that interacts with membrane protein complexes,
transferring electrons between components of the electron transport chain in the
IM. Finally, the IM encloses the matrix compartment, which contains enzymes
of the Krebs cycle and amino acid metabolism, among others. All of these functional compartments are essential to understanding NAD(P)H oxidation by plant
mitochondria. NADH and NADPH can freely pass through the OM (46) but do
not readily penetrate the IM (99). Thus, the pools of NADH and NADPH in the
matrix region are functionally separated from the NADH and NADPH pools of
the intermembrane space-cytoplasm continuum.
The electron transport chain in the IM of plant and animal mitochondria shares
the same basic design. Dehydrogenases (DHs) reduce ubiquinone to ubiquinol that
is oxidized by the cytochrome chain, to finally reduce oxygen to water (Figure 2).
Figure 2 Schematic view of the plant mitochondrial electron transport chain. Multiple
dehydrogenases reduce a common pool of ubiquinone, which is then oxidized by either the
traditional cytochrome pathway or the alternative oxidase.
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MITOCHONDRIAL NAD(P)H DEHYDROGENASES
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The nearly universal DHs, which donate electrons to the ubiquinone pool of the
electron transport chain, are the rotenone-sensitive NADH DH (Complex I), which
oxidizes matrix NADH, and succinate DH (Complex II), which oxidizes the Krebs
cycle intermediate succinate to fumarate. Ubiquinone reduced by these complexes
is oxidized by the cytochrome chain that consists of the bc1 complex (Complex
III), soluble cytochrome c in the intermembrane space, and cytochrome oxidase
(Complex IV). Electron flow through the proton-pumping complexes I, III, and IV
results in the generation of a proton (electrochemical) gradient across the IM. A
large proton gradient limits flow of electrons through the electron transport chain
due to so-called respiratory control. When the established gradient is used to drive
transport processes across the IM, or drive ATP production by the mitochondrial
ATP synthase (Complex V), electron flow through the electron transport chain
increases until the proton gradient is again restricting.
Plant mitochondria have a unique, highly branched respiratory chain with several additional alternative NAD(P)H DHs at the front end and a second, alternative
oxidase in the later part. The alternative NAD(P)H DHs and the alternative oxidase
do not directly contribute to proton pumping or ATP synthesis, so their activities
bypass respiratory control. Since the identification of the alternative oxidase (27),
much knowledge has been acquired on this enzyme, and it has been the subject of
numerous recent reviews (30, 59, 71, 97). The proliferation of alternative NAD(P)H
DHs at the reducing end of the electron transport chain in plants is the primary
focus of this review.
NAD(P)H DEHYDROGENASE ACTIVITIES IN INTACT
MITOCHONDRIA
External NAD(P)H Oxidation
Early investigations of plant mitochondria indicated that they differed from mammalian mitochondria in that they readily oxidized externally added NADH (6, 34,
36). Careful characterization of external NADH oxidation by isolated intact mung
bean mitochondria clearly showed that two NADH DHs were present outside of the
IM barrier (22). One enzyme was localized to the OM, specifically utilized the 4alpha hydrogen of NADH, and did not oxidize NADPH. Low-temperature spectra
indicated that the OM activity contained a flavoprotein and a b-type cytochrome,
and this activity remained firmly associated with the OM during mitochondrial
disruption (22, 73). Comparing enzyme profiles after Pronase treatment of intact
mitochondria suggested that a component of this activity was located on the inner
side of the OM (89). The electron acceptor for this OM DH in situ is not known,
although it has been proposed that it may be cytochrome c, which could functionally link it to the electron transport chain. It was also observed (22) that some
NADH DH activity became solubilized during mitochondrial disruption and that
this activity was specific for the 4-beta hydrogen of NADH. This second activity was proposed to mediate external NADH oxidation. Low-temperature spectra
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indicated that this activity contained a flavoprotein. The release of this activity from
the membrane during mitochondrial disruption made it an attractive candidate for
future purification.
Early reports of external NADH oxidation by isolated plant mitochondria indicated that it had a broad pH optimum near 7, was inhibited by EDTA (ethylenediaminetetraacetic acid), yielded an ADP:O ratio of 1.2 to 1.4, and was inhibited by
the Complex III inhibitor, antimycin A, and by the Complex IV inhibitor, cyanide
(36, 100). ADP:O ratios directly reflect the amount of proton pumping associated
with electron flow, so that ADP:O ratios greater than 2 indicate that electrons are
entering through Complex I. Ratios in the 1.2 to 1.6 range indicate that electrons
enter the electron transport chain just before Complex III. Thus, consistent with the
inhibitor results, external NADH and NAD(P)H DHs feed electrons to ubiquinone.
Subsequently, it was shown that external NADH-dependent oxygen uptake was
stimulated by divalent cations (9, 60). Whereas most cations stimulated by electrostatic screening of negative membrane charges, calcium was specifically required
(26, 62), probably because it affected the interaction with quinone (90). The external NADH DH activity has a high affinity for calcium (70), which is influenced
by polyamines (86, 88).
Red beet roots have been used extensively to study external NADH oxidation.
Mitochondria from fresh tissue either do not oxidize added NADH (16) or do so
poorly (32, 48, 49) compared to other tissues and species. However, this activity can
be induced by slicing and incubating the roots in dilute calcium sulfate solutions
[essentially, recovery from wounding (16, 83)]. Cytoplasmic protein synthesis was
essential for this induction as shown by its abolishment by cycloheximide (12,
83). This induction system has proven useful for characterizing external NADH
oxidation. External NADH oxidation can be induced also by storing harvested red
beet roots at low temperatures (32).
External NADPH-dependent oxygen uptake was initially found to have several
similarities to external NADH oxidation. External NADPH oxidation in isolated
etiolated corn seedling mitochondria was stimulated by calcium, and yielded similar ADP:O ratios to NADH. Also, electron transport chain inhibitors indicated
that electrons from NADPH were donated to ubiquinone (3, 4, 44). However,
NADPH-dependent oxygen uptake in potato tuber mitochondria differs from the
NADH oxidation in some significant aspects. External NADH oxidation occurred
at higher pHs where external NADPH oxidation was minimal. NADPH oxidation
was also much more sensitive to inhibition by EDTA, and was specifically inhibited by several sulfhydryl reagents (4). These results provided initial evidence that
external NADH and NADPH were oxidized by different proteins. In subsequent
papers, pH profiles similar to those from potato mitochondria were observed in
several species and tissues (26, 32, 65, 66). Comparing the pH responses supports the view that more than one protein is involved in the oxidation of external
NAD(P)H. These include NADH-specific enzymes active at neutral pH, as well
as enzymes with optimal pH near 6 that oxidize both NADH and NADPH. Thus,
when external NADH-dependent oxygen uptake is measured, the activity is due to
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MITOCHONDRIAL NAD(P)H DEHYDROGENASES
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more than one DH. It has often been noted that NADPH-dependent oxygen uptake
is inhibited more by EGTA [ethyleneglycol-bis-(β-aminoethyl ether) N,N,N0 ,N0 tetraacetic acid] and stimulated more by calcium than NADH-dependent oxygen
uptake. This suggests that the external NAD(P)H DH enzyme is more calcium
dependent than the external NADH DH enzyme. Consistent with the above, differential expression of external DH activities with diverse NAD(P)H specificity and
calcium dependence have occurred in red beet root and sugar beet root (32, 103).
The NAD(P)H analogs, deamino-NAD(P)H, have been used to investigate
the alternative NAD(P)H DHs of plant mitochondria. In the deamino-analogs of
NAD(P)H, oxygen replaces the free amino group on the adenine ring, limiting
the deamino-analogs’ oxidation to only certain DHs. Intact mitochondria do not
oxidize deamino-NAD(P)H to oxygen, so neither external DH in situ uses the
analogs (57, 69, 80). However if artificial electron acceptors are added to intact
mitochondria, the deamino analogs drive oxygen uptake (57, 69). The resultant
activity may occur because other enzymes become artificially linked to the electron
transport chain, or because of a change in specificity of the NAD(P)H DH(s). When
mitochondria are disrupted, allowing access to the matrix space, deamino-NADH
is readily oxidized. In the absence of artificial electron acceptors, the resultant
oxygen uptake is completely inhibited by rotenone, indicating that it is specific to
Complex I activity (52, 69, 80).
Several attempts have been made to obtain specific inhibitors for the alternative NAD(P)H DHs of plant mitochondria. The general flavoprotein inhibitor,
diphenyleneiodonium (DPI) inhibits external NADPH-dependent oxygen uptake
at much lower concentrations than needed for the external NADH oxidation (52,
84). The flavone platanetin (82, 85) and dicumarol (18, 79) have also shown potential in that they inhibit rotenone-insensitive NAD(P)H DHs, including the external,
with less effect on Complex I. However, none of these inhibitors is strictly specific
to only one NAD(P)H DH, somewhat limiting the inhibitors’ usefulness.
Internal NAD(P)H Oxidation
Another unique feature of plant mitochondria is that oxygen uptake with NADlinked Krebs cycle substrates, presumably via Complex I, was poorly inhibited by
rotenone (38). Rotenone completely inhibits mammalian Complex I, and it was initially unclear why it did not work as well in plant mitochondria. Early investigators
showed that ADP:O ratios dropped to values around 1.5 upon addition of rotenone
(7, 17, 51), indicating that Complex I proton pumping was abolished. However,
kinetic analysis of NADH oxidation in submitochondrial particles suggested that
a rotenone-insensitive matrix-facing NADH DH was present in plant mitochondria in addition to Complex I (67), but with a roughly tenfold lower affinity for
NADH (67, 80, 91). Submitochondrial particles are membrane vesicles formed
upon mitochondrial disruption, and can be largely inside-out if made by sonication under appropriate conditions (63, 74, 80). Using submitochondrial particles
gives NAD(P)H added to the medium access to the matrix surface of the IM, so
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one can directly measure matrix-facing enzymes. During sonication, much of the
external NAD(P)H DH activity is released from the membrane, but any remaining
activity would be internalized and not have access to added NAD(P)H (10, 22, 48,
55, 77, 91).
It is now believed that plant mitochondria contain two internal nonprotonpumping NAD(P)H DHs in addition to Complex I. This is based on NADHand NADPH-dependent oxygen uptake in submitochondrial particles, which have
been characterized by their inhibitor sensitivities (rotenone and DPI), calcium
stimulation, use of deamino-analogs of NAD(P)H, and pH. These characteristics
clearly define the three different matrix-facing NAD(P)H DH activities. Using
the deamino-analogs of NAD(P)H has shown that only Complex I (which greatly
prefers NADH over NADPH) can oxidize the analogs under these conditions, and
that rotenone completely inhibits the resultant oxygen uptake. Subsequent addition
of normal NADH or NADPH results in resumed oxygen uptake driven by alternative internal NAD(P)H DHs (57, 80). Under these conditions, NADPH-dependent
oxygen uptake is stimulated by calcium (79) and inhibited by the general flavoprotein inhibitor DPI (1, 52). In contrast, NADH-dependent oxygen uptake under
the same conditions was affected by neither calcium nor DPI. These experiments
provide conclusive evidence for the two alternative internal NAD(P)H DHs. One
is specific for NADH; the other oxidizes NADPH and possibly also NADH.
EFFORTS TO PURIFY ALTERNATIVE NAD(P)H
DEHYDROGENASES
Early characterization of external NAD(P)H oxidation suggested that the DHs involved are loosely associated with the outer surface of the IM, and released into
solution upon disruption of mitochondria (22). This observation formed the basis
for efforts to purify the DH proteins from the soluble protein fraction of disrupted
plant mitochondria. Several early purification efforts with different species indicated that 2 or 3 NAD(P)H DH activities could be separated from soluble fractions
of plant mitochondria (8, 11, 13–15, 42). With the development of FPLC systems,
efforts of several research groups focused on purifying the proteins responsible for
these activities. After several years, four different proteins emerged as potential
alternative NAD(P)H DHs.
A protein of 32 kDa that oxidized NADH was purified and localized to the
outer surface of the IM or to the intermembrane space (43, 49). This protein reduced quinones at a high rate, was not stimulated by calcium, and was severely
inhibited by dicumarol and the sulfhydryl reagents p-chloromercuribenzoic acid
and mersalyl. The 32 kDa-NADH DH has a pH optimum near 7. Recently, this
protein (and its gene) was identified by mass spectrometry and was closely related to the cytochrome b5 reductases (A.J. Liska, D.M. Rhoads, A. Shevchenko
& T.E. Elthon, unpublished results), and very similar to the yeast MCR1 protein (35). It was recently shown that yeast MCR1 can catalyze reduction of the
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MITOCHONDRIAL NAD(P)H DEHYDROGENASES
29
D-erythroascorbyl free radical, and thus may play a critical role in protection
against reactive oxygen species (45).
A protein of 43 kDa, with both NADH and NADPH DH activity, was purified
from red beet roots (49, 56). This protein was localized to the inner surface of the IM
(56). Thus, the 43-kDa protein may be an internal rotenone-insensitive NAD(P)H
DH. This 43-kDa DH reduced quinones at a high rate, and was more sensitive
to dicumarol than to p-chloromercuribenzoic acid. A similar 43-kDa protein has
not been found in maize soluble extracts (47), but has been isolated from potato
mitochondria (54). The gene for the 43-kDa NAD(P)H DH has yet to be identified.
A potential NAD(P)H DH of 58 kDa has been isolated from red beet root
and maize. In red beet root mitochondria, the activity was purified to a 58-kDa
protein doublet that was specific for NADH. The activity was inhibited by pchloromercuribenzoic acid and mersalyl, and by the flavone platanetin (48, 49).
In maize, the partially purified enzyme oxidized both NADH and NADPH, and
with similar inhibition characteristics. Antibodies against the beet 58-kDa protein doublet were used to show that much of the protein in maize was localized
to the outer surface of the IM or to the intermembrane space. The 58-kDa protein doublet from red beet root contained two NADH DH activities that could be
separated by blue-affinity chromatography (55). One of these activity peaks is the
L-protein of the pyruvate DH, glycine DH, and 2-oxoglutarate DH complexes. This
is based on arsenite-sensitive lipoamide reductase activity (55, 78), and N-terminal
sequence information obtained from the purified red beet root doublet. The other
activity separated by blue-affinity chromatography is likely a viable candidate
for an external NADH DH. It is inducible in aged red beet root tissues. Surprisingly, the purified protein also oxidized NADPH even though only NADH activity
(in situ) was induced by aging (55). The gene for this 58-kDa NADH DH remains
to be determined.
A fourth potential NAD(P)H DH activity was purified from red beet root mitochondria to a 26-kDa protein (78). This potential DH oxidized both NADH and
NADPH, and may be a trimer or tetramer in its native state. A similar 26-kDa
NAD(P)H DH was isolated from beet root cytoplasm (96), indicating that this
protein probably is a soluble NAD(P)-linked DH present in several compartments
of the cell.
Comparing soluble NAD(P)H DH preparations from etiolated maize seedling
shoots, etiolated wheat seedling shoots, and aged beet roots indicated that protein
amounts varied with species (47). Differences between reported activity profiles
in isolated mitochondria may reflect species-specific protein expression levels. It
is also clear that single amino acid substitutions in proteins may alter the conformation around the NAD(P)H-binding site, changing their specificity for NADH
and NADPH and affecting calcium affinity (29, 31). Possibly, the release of DHs
from the membrane constitutes a conformational change with a similar effect,
making the distinct diagnostics of purified proteins more difficult. Furthermore,
soluble NAD(P)-linked DHs may catalytically mimic membrane-bound NAD(P)H
DHs after solubilization, as illustrated by L-protein NADH:quinone oxidoreductase
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activity. Thus, the genes for the purified potential DHs need to be identified to help
determine their role, if any, in NAD(P)H-dependent oxygen uptake.
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PLANT HOMOLOGS OF BACTERIAL AND FUNGAL
NAD(P)H DEHYDROGENASES
Type II NAD(P)H DHs carry out rotenone-insensitive NAD(P)H:ubiquinone reductase activity in bacteria and in fungal mitochondria (39, 98, 101). The latter
include internal NADH DHs, working in parallel with Complex I or alone [e.g.,
Saccharomyces cerevisiae NDI1 (20)] and also external NADH and NADPH DHs
[e.g., S. cerevisiae NDE proteins and Neurospora NDE1 (50, 53)]. These Type II
NAD(P)H DHs typically have a molecular mass around 50 kDa and contain flavin
adenine dinucleotide as a prosthetic group. Two potato gene homologs of this superfamily, nda1 and ndb1, encode mitochondrial proteins localized to the internal
and external side of the IM, respectively (77, 81). Homologs to Type II NAD(P)H
DHs are also present in Arabidopsis and rice and the encoded plant proteins show
high-sequence similarity to the potato proteins NDA1 and NDB1 (58, 72). Thus,
there are two families in plants that correspond to nda(I) and ndb(E), where (I)
and (E) denote their putative, though not fully demonstrated, internal and external
localization, respectively. (Proteins and genes with determined location are here
denoted with an ultimate I or E.) Based on sequence similarities, in Arabidopsis,
two nda(I) genes and four ndb(E) genes are present. (Follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org
to see Table 1.)
The NDA(I) proteins of potato and Arabidopsis have calculated molecular
masses of 55–57 kDa, but the potato NDA1I is processed upon import and has
an apparent molecular mass of 48 kDa (81), which agrees best in size with the
43-kDa protein isolated from beet root and potato tuber mitochondria (48, 49, 54,
56). However, the NDA1I protein remains firmly bound to the membrane upon
sonication (81), similar to the S. cerevisiae NDI1 and Escherichia coli NDH proteins. The NDA(I) proteins likely oxidize matrix NADH, based on the internal
localization of potato NDA1I, the absence of any potential calcium-binding domain, and correlation of activity with expression of the potato nda1I (58, 77, 81,
93, 94). Also, analyzing T-DNA insertion mutants in Arabidopsis recently identified At-NDA1 (referred to as AtNDI1 in 72) as an internal NAD(P)H DH (72).
Mitochondria isolated from the mutant plants showed no difference in Complex
I activity or OM-associated NAD(P)H oxidation, compared to wild-type plants.
However, internal rotenone-insensitive NADH oxidation decreased by 60–70%
and external NAD(P)H oxidation increased by 300–400%. In vitro import experiments showed that the At-NDA1I was imported to the matrix side of the IM as a
protein with an apparent molecular mass of 56 kDa. The residual, internal NADH
oxidation, provides evidence for the presence of additional internal NAD(P)H
DH(s).
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The Arabidopsis NDB(E) proteins have molecular masses of 63–65 kDa, including the putative presequences. However, presequence processing was not detected for the potato NDB1E which has a molecular mass of 61 kDa, according
to SDS-PAGE (81, 94). E. coli-expressed potato NDB1E, as well as antibodydetected mitochondrial NDB-proteins, are loosely associated with the mitochondrial membrane (77, 81). The potato ndb1E has been overexpressed in Nicotiana
sylvestris with transgenic lines showing elevated or suppressed oxidation of external NADPH, but no changes in external nor internal NADH oxidation, indicating
that potato NDB1E oxidizes external NADPH (A.M. Michalecka, S.C. Agius,
I.M. Møller & A.G. Rasmusson, unpublished observations). Arabidopsis has four
ndb(E) genes, all potential external NAD(P)H DHs, but it is possible that one
of the ndb genes encodes an internal enzyme, catalyzing the calcium-dependent
oxidation of matrix NAD(P)H. The similarity in molecular mass and membrane
association to the 58-kDa NAD(P)H DH proteins purified from maize and red beet
roots (48, 55) indicates that these proteins may be of the NDB type.
A more distantly related NAD(P)H DH family, ndc, is present in Arabidopsis
and rice, and the At-NDC1 protein is mitochondrially localized by green fluorescent
protein fusion analysis (58). This third gene family for mitochondrial NAD(P)H
DHs is most closely related to cyanobacterial NAD(P)H DH genes, indicating that
an ndc gene likely entered the eukaryotic cell via the chloroplast genome, and later
transferred to the nucleus where it acquired presequences specifying mitochondrial
targeting (58). The function and intramitochondrial location of the NDC1 protein,
external or internal, is not known.
Plant NDA(I) and NDB(E) proteins have a common origin with the fungal
homologs. (Follow the Supplemental Material link from the Annual Reviews home
page at http://www.annualreviews.org to view Figure 3.) The genes partition into
three clades, containing NDA(I), NDB(E), and most fungal homologs, respectively.
Additionally, the NDI1 and NDE1 of Neurospora, and most protist proteins are
not clearly associated with any of these three clades. The NDA(I) proteins of
potato and Arabidopsis associate strongly with one of the two rice homologs. The
NDB(E) proteins appear to partition into at least three groups. One group contains
homologs of monocotyledons, one dicotyledonous, and one may contain homologs
of both plant classes, including the potato NDB1E. The large cluster of NDB(E)
proteins is consistent with the multitude of external NAD(P)H DH activities found
in mitochondria of both dicotyledons and monocotyledons. Early duplications of
nda(I) and ndb(E) genes indicate that the genes may have developed functional
specializations in the organism of the common origin. However, it is not clear if
function and localization are reflected in the relationships between the proteins. In
the fungal clade, for example, the external DHs in S. cerevisiae and Yarrowia group
separately. Additionally, the Sc-NDE-proteins have a common origin with the
internal Sc-NDI1, indicating that a change in intramitochondrial targeting occurred
in the evolution of either protein(s). Such protein redirection has been accomplished
experimentally where the external NDH2 of Yarrowia was retargeted to the internal
side of the IM by genetically modifying the presequence (40).
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The functional domains of NAD(P)H DH sequences found in bacteria and
fungi are conserved in the plant families. An N-terminal region is likely involved
in targeting to the mitochondrion and intramitochondrial sorting. Two nucleotidebinding motifs are most likely involved in binding flavin adenine dinucleotide and
NAD(P)H. The C terminus may take part in membrane binding as suggested by
membrane association of potato NDA1I overexpressed in E. coli (81). In addition
to the common domains, the plant NDB(E) family contains an insert carrying a
single EF-hand motif (81), suggesting that this domain binds calcium, which is
known to activate the external NAD(P)H DHs.
At this stage all the genes/proteins responsible for the NAD(P)H DH activities
in situ are not known. The available evidence most clearly suggests that the NDA1I
proteins of potato and Arabidopsis are internal NADH DHs and that potato NDB1E
is involved in external NADPH oxidation, leaving several activities unaccounted
for. It is not clear why there are so many homologs of these genes in Arabidopsis and
rice. They could represent isoforms expressed in a tissue-specific or developmental
pattern or they could represent a level of redundancy in the genomes. Using genetic
approaches to identify the proteins and genes involved in alternative NAD(P)H
oxidation will continue to be a successful strategy to answer these questions. The
potential roles of the purified NAD(P)H DH activities need to be re-evaluated
following identification of their genes.
PHYSIOLOGICAL ROLES OF ALTERNATIVE NAD(P)H
DEHYDROGENASES
Although external NAD(P)H oxidation has been known for a long time, its physiological importance is still not understood. For example, the physiological relevance of the most studied induction system, red beet root (see above), is not
known. Potentially, the external NAD(P)H DHs may regulate the reduction state
of the cytoplasmic pools of NADH and NADPH in response to variations in calcium concentration. This could in turn influence flux through pathways of primary carbon metabolism, nitrogen assimilation, NADPH-dependent pathogenic
responses, biosynthetic pathways, and intracellular redox shuttles (35a, 44a). However, whether such regulation takes place in vivo is not known, and data obtained
with transgenic or mutant systems are needed for evaluating these possible roles.
For example, in the Arabidopsis nda1I mutant, total matrix NAD(P)H oxidation
was reduced and activity of the external NAD(P)H DHs increased dramatically
(72). This may be a compensatory response with matrix-reducing equivalents being exported via a malate/oxaloacetate shuttle (19). A similar increase in external
NADH oxidation has also been observed in Complex I mutants (33) and indicates
a role of these DHs in maintaining the redox balance of the cell.
Linking any of the alternative mitochondrial DHs with the alternative oxidase
results in electron flow to oxygen without proton pumping and thus no oxidative phosphorylation. Several hypotheses relating to the physiological roles of the
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MITOCHONDRIAL NAD(P)H DEHYDROGENASES
33
alternative oxidase (59, 97) can also be applied to alternative NAD(P)H DHs, such
as thermogenesis, oxidation of excess carbohydrates, oxidation of excess reductant for continuation of metabolic pathways, cold resistance, phosphate deficiency,
and avoidance of reactive oxygen species formation. These need to be experimentally tested in each case. A general role, relevant for all energy-independent pathways, may reside in the simplicity of the enzymes as compared to the complexes
they bypass. Plants experience large and rapid shifts in their environment, affecting metabolism. Up- and down-regulation of electron transport pathways to meet
short-term needs may be more efficiently carried out by expressional modulation of
the simpler alternative enzymes, as previously suggested for fungal mitochondria
(39). Under different physiological conditions specific alternative NAD(P)H DHs
may be expressed and potentially linked to the alternative oxidase. For example,
when tobacco cells were grown in phosphate-limited media there was an increase
in rotenone-insensitive malate oxidation and external NADH DH activity (K.L.
Soole, unpublished observations), as well as an increase in alternative oxidase activity (75). This indicates a coordinated response of nonphosphorylating pathways,
relieving the respiratory control restriction imposed by the lack of phosphate, a
substrate for ATP synthesis.
It was recently shown that expression of the potato nda1I gene depends on light
regulated in a circadian fashion, and that this expression correlates with increased
internal rotenone-insensitive NADH oxidation and alternative oxidase protein (94).
These results indicate that this alternative DH is important for photosynthetically
associated metabolism, most likely photorespiration. Previous investigators have
shown low rotenone sensitivity for glycine oxidation in leaf mitochondria from several species (21, 37). Work with Complex I mutants have consistently demonstrated
the importance of unperturbed oxidation of matrix NADH for chloroplast function
(25, 87). Under photorespiratory conditions, it is likely that an internal NADH DH
operates in consort with the alternative oxidase to oxidize excess NADH, bypass
ATP synthesis, and allow continued flux through the photorespiratory cycle.
During cold treatment of potato leaves, internal rotenone-insensitive NADH oxidation in mitochondria decreased, which correlated with lower NDA1(I) protein
and mRNA levels (93). This may be due to abolishment of photorespiration in the
cold. Alternatively, the decrease in NDA1 may have a redox-balancing function.
Cold stress elevates alternative oxidase expression and reactive oxygen species
levels in plants (59). It has been suggested that the alternative oxidase maintains the redox balance of the ubiquinone pool, thus minimizing the formation
of reactive oxygen species from reduced ubiquinone (76). Similarly, NAD(P)H
DHs may be involved in redox balancing. A decrease in expression of alternative NAD(P)H DHs may lower the reduction state of the ubiquinone pool. In this
case, the redox state of the ubiquinone pool would be regulated at both reducing
and oxidizing sides, analogous to the situation for plastoquinone in thylakoids
where redox control regulates synthesis and activity of quinone-reducing and
-oxidizing photosystems (2). Recent results with N. sylvestris mutants for Complex I subunits additionally suggest that changes in mitochondrial NAD(P)H
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oxidation can influence the redox poise of other cellular compartments, including
the chloroplast (25).
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CONCLUDING REMARKS
The plant mitochondrial electron transport chain is more complex than first envisioned, and is more reminiscent of its fungal counterparts. Varied expression and
activity of the alternative NAD(P)H DHs and the alternative oxidase provides remarkable flexibility in regulating the redox state of cytoplasmic and mitochondrial
matrix NAD(P)H pools. Plants clearly have the need to oxidize excess NAD(P)H,
and do so by bypassing the universal electron transport chain and its inherent
coupling to ATP synthesis.
ACKNOWLEDGMENTS
The authors thank Ian M. Møller and David A. Day for critically evaluating
the manuscript. A.G.R. acknowledges support from the Swedish Research Council for Environment, Agricultural Sciences, and Spatial Planning, and Carl Tesdorpfs Stiftelse. K.L.S. acknowledges support from the Australian Research
Council.
The Annual Review of Plant Biology is online at http://plant.annualreviews.org
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MITOCHONDRIAL NAD(P)H DEHYDROGENASES
C-1
Figure 1 Membrane model of the plant mitochondrial electron transport chain. Alternative
NAD(P)H dehydrogenases and the alternative oxidase are shown in green.
P1: FRK
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Annual Review of Plant Biology
Volume 55, 2004
CONTENTS
Annu. Rev. Plant Biol. 2004.55:23-39. Downloaded from arjournals.annualreviews.org
by CAPES on 10/30/08. For personal use only.
AN UNFORESEEN VOYAGE TO THE WORLD OF PHYTOCHROMES,
Masaki Furuya
1
ALTERNATIVE NAD(P)H DEHYDROGENASES OF PLANT
MITOCHONDRIA, Allan G. Rasmusson, Kathleen L. Soole,
and Thomas E. Elthon
DNA METHYLATION AND EPIGENETICS, Judith Bender
PHOSPHOENOLPYRUVATE CARBOXYLASE: A NEW ERA OF
STRUCTURAL BIOLOGY, Katsura Izui, Hiroyoshi Matsumura,
Tsuyoshi Furumoto, and Yasushi Kai
METABOLIC CHANNELING IN PLANTS, Brenda S.J. Winkel
RHAMNOGALACTURONAN II: STRUCTURE AND FUNCTION OF A
BORATE CROSS-LINKED CELL WALL PECTIC POLYSACCHARIDE,
Malcolm A. O’Neill, Tadashi Ishii, Peter Albersheim, and Alan G. Darvill
23
41
69
85
109
NATURALLY OCCURRING GENETIC VARIATION IN ARABIDOPSIS
THALIANA, Maarten Koornneef, Carlos Alonso-Blanco, and
Dick Vreugdenhil
141
SINGLE-CELL C4 PHOTOSYNTHESIS VERSUS THE DUAL-CELL (KRANZ)
PARADIGM, Gerald E. Edwards, Vincent R. Franceschi,
and Elena V. Voznesenskaya
173
MOLECULAR MECHANISM OF GIBBERELLIN SIGNALING IN PLANTS,
Tai-ping Sun and Frank Gubler
PHYTOESTROGENS, Richard A. Dixon
DECODING Ca2+ SIGNALS THROUGH PLANT PROTEIN KINASES,
Jeffrey F. Harper, Ghislain Breton, and Alice Harmon
PLASTID TRANSFORMATION IN HIGHER PLANTS, Pal Maliga
SYMBIOSES OF GRASSES WITH SEEDBORNE FUNGAL ENDOPHYTES,
Christopher L. Schardl, Adrian Leuchtmann, Martin J. Spiering
197
225
263
289
315
TRANSPORT MECHANISMS FOR ORGANIC FORMS OF CARBON AND
NITROGEN BETWEEN SOURCE AND SINK, Sylvie Lalonde,
Daniel Wipf, and Wolf B. Frommer
341
vii
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CONTENTS
REACTIVE OXYGEN SPECIES: METABOLISM, OXIDATIVE STRESS,
AND SIGNAL TRANSDUCTION, Klaus Apel and Heribert Hirt
THE GENERATION OF Ca2+ SIGNALS IN PLANTS,
Alistair M. Hetherington and Colin Brownlee
BIOSYNTHESIS AND ACCUMULATION OF STEROLS, Pierre Benveniste
HOW DO CROP PLANTS TOLERATE ACID SOILS? MECHANISMS OF
ALUMINUM TOLERANCE AND PHOSPHOROUS EFFICIENCY,
Annu. Rev. Plant Biol. 2004.55:23-39. Downloaded from arjournals.annualreviews.org
by CAPES on 10/30/08. For personal use only.
Leon V. Kochian, Owen A. Hoekenga, and Miguel A. Piñeros
VIGS VECTORS FOR GENE SLIENCING: MANY TARGETS,
MANY TOOLS, Dominique Robertson
GENETIC REGULATION OF TIME TO FLOWER IN ARABIDOPSIS THALIANA,
Yoshibumi Komeda
373
401
429
459
495
521
VISUALIZING CHROMOSOME STRUCTURE/ORGANIZATION,
Eric Lam, Naohiro Kato, and Koichi Watanabe
537
THE UBIQUITIN 26S PROTEASOME PROTEOLYTIC PATHWAY,
Jan Smalle and Richard D. Vierstra
555
RISING ATMOSPHERIC CARBON DIOXIDE: PLANTS FACE THE FUTURE,
Stephen P. Long, Elizabeth A. Ainsworth, Alistair Rogers,
and Donald R. Ort
591
INDEXES
Subject Index
Cumulative Index of Contributing Authors, Volumes 45–55
Cumulative Index of Chapter Titles, Volumes 45–55
ERRATA
An online log of corrections to Annual Review of Plant Biology
chapters may be found at http://plant.annualreviews.org/
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