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First published online May 29, 2009; 10.1104/pp.109.139782 Plant Physiology 150:1286-1296 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
The Transcription Factor ABI4 Is a Regulator of Mitochondrial Retrograde Expression of ALTERNATIVE OXIDASE1a1,[C],[W],[OA]Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley 6009, Western Australia, Australia
Plant cells integrate signals from external sources and from organelles to regulate gene expression, referred to as anterograde and retrograde signaling, respectively. Functional characterization of the promoter of ALTERNATIVE OXIDASE1a (AOX1a) from Arabidopsis (Arabidopsis thaliana), a marker for mitochondrial retrograde response, was carried out by testing the ability of the AOX1a promoter to drive expression of the reporter gene GUS. This approach identified a strong repressor element, designated the B element, that was necessary for an increased promoter activity in response to the mitochondrial complex I inhibitor rotenone. This element overlaps with a previously identified potential binding site for the transcription factor ABSCISIC ACID INSENSITIVE4 (ABI4). AOX1a promoter activity was fully derepressed in abi4 mutants and was unresponsive to rotenone. Furthermore, deletion of the B element of the AOX1a promoter resulted in increased GUS staining activity compared to the wild-type promoter in transgenic plants. Binding of the ABI4 transcription factor to this region of the AOX1a promoter was demonstrated by electromobility shift and yeast one-hybrid assays. Analysis of transcript abundance for AOX1a in abi4 mutant lines revealed significantly increased levels of AOX1a mRNA that could not be further induced by rotenone, consistent with the role of ABI4 as a repressor that is derepressed in response to rotenone. These results show that ABI4 plays a central role in mediating mitochondrial retrograde signals to induce the expression of AOX1a. Furthermore, they provide a molecular link between mitochondrial and chloroplast retrograde signaling, as ABI4 has been previously shown to act downstream of at least two chloroplast retrograde signaling pathways.
The alternative oxidase (AOX) is a cyanide-insensitive terminal oxidase found in all plants studied to date (Vanlerberghe and McIntosh, 1997  ). Although the activity was known to exist more than 100 years ago (for review, see Moore and Siedow, 1991), research into the nature of this activity was greatly facilitated by the development of a monoclonal antibody that recognized AOX from a wide variety of species (Elthon et al., 1989) and cloning of the cDNA from Sauromatum guttatum (Rhoads and McIntosh, 1991) that facilitated the cloning of cDNA from a variety of other plant species. In higher plants, AOX is encoded by a small gene family, with the number of genes varying between species. AOX has been studied at an activity, protein, and gene level (Finnegan et al., 2004), and these studies reveal that its expression at an mRNA level is induced by a variety of treatments that are commonly referred to as stresses. Expression in a variety of organs at various developmental stages is also observed. At a protein level, AOX in plants can exist as an oxidized dimer (inactive) via intermolecular disulphide cross-linking of conserved Cys residues, and pyruvate and a variety of other  -keto acids act as allosteric activators (Umbach et al., 1994). However, the in vivo implications of these potential posttranscriptional regulatory mechanisms are still unclear.
In addition to the fact that AOX represents a biochemical feature of the plant mitochondrial electron transport chain (mETC), it is also the preeminent model for mitochondrial retrograde regulation in plants (Rhoads and Subbaiah, 2007
In chloroplasts, four distinct retrograde signals have been characterized: signals resulting from the inhibition of plastid gene expression, Mg-protoporphyrin IX (Mg-proto) accumulation, chloroplast-generated reactive oxygen species, and REDOX signals from the photosynthetic electron transport chain (Butow and Avadhani, 2004
In yeast, mitochondrial dysfunction leads to activation of a retrograde pathway where a variety of genes are activated by binding of the retrograde regulatory factors 1 and 3 to an R box (GTCAC) in their promoters (Liu and Butow, 1999 In this study, we show that the transcription factor ABI4 is involved in the retrograde regulation of AOX1a in Arabidopsis. A combined approach of functional analysis of cis-acting regulatory elements in the upstream region of AOX1a, yeast one-hybrid assays, electro-mobility shift assays (EMSA), and use of ABA-insensitive signaling mutants all reveal a central role for ABA response factors in the regulation of AOX1a.
The AOX1a Promoter Contains a Sequence Element That Represses Promoter Activity
Previous studies on the promoter region of AOX1a revealed that it was responsive to the addition of various compounds, including the mETC complex I inhibitor rotenone (Ho et al., 2008
The AOX1a Promoter Region Contains cis-Acting Regulatory Elements That Are Potential Binding Sites for ABA Response Factors
In the context of the AOX1a promoter, the B element overlaps with a potential binding site for ABI4, the coupling element CE1 (CACCG; Niu et al., 2002
A possible role for the transcription factor abi3 in regulating AOX1a promoter activity was also examined, as it has also been shown to bind an ACGTG promoter motif containing the same CGTG core sequence as the B element (Roschzttardtz et al., 2009
As abi3 and abi4 were originally characterized as having alterations in ABA responses and since ABA is a known stress hormone, the ability of the AOX1a promoter to respond to ABA treatment was tested. The ability of the AOX1a promoter (wild-type and with the B element deleted) to drive GUS reporter gene expression was tested by transient transformation of Arabidopsis leaf tissue after 3 h of pretreatment with 100 µM ABA. However, a negative response of the promoter was observed (data not shown). This may be due to technical limitations of the transient transformation process; leaves are detached from the plant affecting stomatal closure, which has been linked to ABA signaling and assayed for activity 27 h later. The transformation process in itself can be a significant stress on the plant (Ho et al., 2008 It was concluded that element B played an essential role in the ability of the AOX1a promoter to respond to rotenone. A functional ABI4 appeared to be necessary for this response, as in the absence of ABI4, the AOX1a promoter displayed a very high activity. Thus, under normal growth conditions AOX1a was under negative regulation.
To test if the ABI4 transcription factor binds to the region of the B element in the AOX1a promoter, a 50-bp region surrounding the B element as shown in Figure 1A was used as a bait for binding assays in the yeast one-hybrid system (Vidal and Legrain, 1999
To further assess the binding of ABI4 and ABI3 to the AOX1a B element region, EMSAs were performed. A biotin-labeled double-stranded DNA probe containing the 50-bp region surrounding the AOX1a B element was synthesized, whereas the transcription factors were expressed in an in vitro translation system. The labeled probe was incubated with and without transcription factor protein extracts and separated on native polyacrylamide gels. In a third reaction, an excess of unlabeled DNA probe competitor was added to the incubation mixture to verify if the interaction and observed shifts were specific. For ABI3, we were unable to show specific shifts using EMSAs and could not further confirm binding to the B element region (data not shown). For ABI4, shifted bands were routinely observed with the ABI4 and AOX1a B element oligonucleotide that could be abolished using a competitor against the whole 50-bp region (Fig. 4 ). Assays were also performed using specific competitors for each of both ABI4 binding sites. As each competitor was able to abolish one specific shift, these assays confirmed the specific binding of ABI4 to both putative ABI4 binding sites in the promoter of AOX1a. Thus, it was concluded that the ABI4 transcription factor binds to the B element region in the AOX1a promoter.
Transcript Abundance of AOX1a Is Responsive to ABA and Affected by ABI4 As both transcription factors ABI3 and ABI4 were originally isolated for their reduced sensitivity to ABA application, it was investigated if transcript abundance of AOX1a is directly responsive to ABA and if the increase in transcript abundance of AOX1a observed in response to rotenone is affected by the absence of ABI3 or ABI4. Transcript abundance of AOX1a was analyzed by quantitative reverse transcription-PCR (QRT-PCR) and was found to be strongly induced after treatment with ABA (Fig. 5 ). To confirm that AOX1a gene expression in response to ABA and rotenone is subjected to regulation by ABA signaling factors in planta, transcript levels were analyzed in the abi3 and abi4 signaling mutants using two different mutant alleles of each gene. In the case of abi4 mutant backgrounds, AOX1a transcripts displayed a 2-fold increase in abundance (Fig. 5). Furthermore, the significant increase in transcript abundance by rotenone or ABA treatment was abolished, likely due to the fact that the uninduced transcript abundance in the abi4 mutant backgrounds was as high as the induced levels of transcript abundance in the Col-0 background, indicating the expression could not be further derepressed in the mutant upon stress treatment. Transcript abundance in abi3 mutant backgrounds was not significantly different compared to the wild type (Landsberg erecta [Ler]), in agreement with the promoter activity (Fig. 1B). Furthermore, an increase in transcript abundance for AOX1a with rotenone and ABA treatment was not abolished in the abi3 mutant backgrounds. In summary, AOX1a transcript abundance is induced by ABA and by rotenone, and ABI4 appears to play an essential role in the response to these signals.
Multiple lines of evidence point to a role for the ABI4 transcription factor in the regulation of AOX1a in response to retrograde signals. Deletion of the B element in the AOX1a promoter and the absence of the ABI4 transcription factor have similar effects on promoter activity: the promoter is derepressed and loses ability to respond to rotenone. Additionally, transcript abundance for AOX1a increased in abi4 mutant lines and was unresponsive to rotenone. The ABI4 transcription factor was shown to interact with AOX1a in two binding assays, EMSA and yeast one-hybrid assay, respectively, indicating that is directly involved in AOX1a transcription.
The finding that AOX1a is repressed by ABI4 is consistent with previous studies on AOX. Arabidopsis plants with a T-DNA insertional mutation of aox1a display increased sensitivity to stress and have altered levels of several genes involved in anti-oxidant defense (Giraud et al., 2008
Previous characterization of the AOX1a promoter from Arabidopsis identified a region that contained putative binding sites for WRKY and Dof transcription factors (Dojcinovic et al., 2005
Regulation of the expression of AOX1a via ABI4 provides a direct link between chloroplast and mitochondrial retrograde signaling (Koussevitzky et al., 2007
ABA signaling factors have also been found to be closely associated with sugar signaling, for example, abi4 mutants are allelic to multiple Glc-insensitive mutants (Rook et al., 2006 ; Bossi et al., 2009), and ABI3 has also been found to function in Glc signaling (Dekkers et al., 2008). Glc is an early inducer of AOX1a expression (Li et al., 2006), suggesting that not only ABA but also carbohydrate signals could be integrated through ABI3-4 regulation. As photosynthesis supplies plants with sugars, it seems quite useful that regulation of chloroplast function, carbohydrate metabolism, and mitochondrial respiration share common regulatory factors. Although ABI3 appears to be a negative regulator of photosynthetic genes, and possibly displays a GUN phenotype (our interpretation of data presented in Fig. 3A in Koussevitzky et al., 2007), ABI3 appears to be a positive regulator of AOX1a (Fig. 6), as evidenced by the fact that it was necessary for the increase in AOX1a promoter activity when the B element was deleted (Fig. 1C).
A connection between mitochondrial and chloroplast retrograde signaling also indicates that signals from both organelles interact. A mutation in Arabidopsis prolyl-tRNA synthetase that is targeted to mitochondria and plastids that results in decreased rates of organelle translation causes a decrease in transcript abundance for nuclear genes encoding proteins involved in photosynthesis (Pesaresi et al., 2006
Plant Material Growth and Treatments Arabidopsis (Arabidopsis thaliana) mutant lines were obtained from the Arabidopsis Biological Resource Center at The Arabidopsis Information Resource: abi3-4, CS6130; abi3-5, CS6131; abi4-1, ABI4-1BPS1-2; abi4-102, CS3837. Arabidopsis plants, ecotype Col-0, Ler, and corresponding mutant lines were grown at 22°C for 16 h at 100 µE m–2 s–1 light conditions and 8 h of dark. For treatments, Arabidopsis leaf tissue was taken from 4-week-old plants. Stems of each leaf were submerged into the mock (same volume of water or ethanol solvent for stress solution added) or treatment solution for 3 h. A final concentration of 40 µM was used for rotenone and 100 µM for ABA.
QRT-PCR was performed on Arabidopsis tissue from abi3 (abi3-4 and abi3-5) and abi4 (abi4-1 and abi4-102) mutant lines, and their respective wild-type ecotypes Ler and Col-0. Seedlings were cultivated in vitro on Murashige and Skoog media and harvested at developmental stage 1.04 (Boyes et al., 2001
The promoter regions were cloned using standard protocols and subcloned into pLUS (see Supplemental Table S1 for primer sequence). The numbering of Arabidopsis AOX1a promoter is given from the transcriptional start site as determined from the SIGAL database (Yamada et al., 2003
Promoter regions were subcloned into pCAMBIA1301 (http://www.cambia.org/daisy/cambia/585.html), using standard protocols, as a translational fusion with GUS. Six-week-old Arabidopsis plants were transformed using Agrobacterium tumefaciens-mediated transformation of the flowers (Clough and Bent, 1998
Transformation was performed using the PDS-1000 system using the Hepta adaptor according to the manufacturer's instructions (Bio-Rad) as previously described (Ho et al., 2008 Standard errors are shown, and to determine statistical significance, a Student's t test was performed assuming unequal variances. For comparison of GUS activities of the motif deletions with that of the unmutated promoter, a two-sample t test assuming unequal variances was also performed. Significance was defined as P # 0.05. The following comparisons were carried out to determine the activity of each element tested: (1) A comparison of the normalized GUS activity between the wild-type promoter and the mutated promoter; this determined if the element has any regulatory function in the absence of any stress treatment. Significance for this is indicated with a red asterisk. (2) A comparison between the mock-treated and stress-treated GUS values. This determines if the promoter fragment was stress responsive and if deleting the element resulted in a loss of a significant effect. Significance for this is indicated with a black asterisk. (3) A comparison between the treated GUS values of the wild-type promoter in wild-type plants compared to mutant plants. This determines if promoter activity is altered in a mutant. Significance for this is indicated with a green asterisk.
The coding regions of the transcription factors ABI3 (At3g24650) and ABI4 (At2g40220) were cloned from Arabidopsis Col-0 cDNA using standard protocols with the Roche Expand High Fidelity PCR system (Roche), using gene specific primers (Invitrogen). The PCR products were then cloned into the pGADT7-rec2 prey vector (CLONTECH), creating a translational fusion between the GAL4 activation domain and the transcription factor. As a control system, the binding capacity of the p53 transcription factor to a DNA sequence containing (p53 +) or not containing (p53 –) a p53-binding motif was used. For construction of the pHIS2 bait vectors, forward and reverse oligonucleotides (Supplemental Table S1) were annealed and subcloned into EcoRI/SacI linearized pHIS2 vector. The 50-bp sequence surrounding the B element was cloned into the pHIS2 reporter vector upstream of the minimal HIS3 promoter region and HIS3 nutritional reporter gene. Similarly, a synthetic construct containing three consecutive repeats of the B element was cloned into the pHIS2 vector.
Competent yeast cells were prepared according to the CLONTECH Yeast Protocols Handbook using the Y187 yeast strain. Yeast one-hybrid transformation screens were performed using the CLONTECH Matchmaker One Hybrid Library Construction and Screening kit. For each yeast one-hybrid transformation screen, 100 µL of competent yeast cells were incubated with 100 ng of pHIS2 bait vector and 100 ng of pGADT7-Rec2 prey vector, 100 µg Herring Testes Carrier DNA (CLONTECH), and 0.6 mL PEG/LiAc solution. Cells were transformed according to the manufacturer's instructions. Transformations were plated onto SD media –Leu –Trp to select for cotransformed cells and incubated at 28°C for 4 d. The pGADT7-rec2-p53 prey vector in combination with p53HIS2 was used as a positive control transformation and pGADT7-rec2-p53 in combination with pHIS2 as negative control. Transformed yeast cells were subsequently grown in SD –Trp –Leu liquid media to OD600 of 0.1 and diluted in a 10x dilution series. From each dilution, 5 µL was spotted on SD –Trp –Leu and on SD –Trp –Leu –His media plates supplemented with 75 or 90 mM 3AT (Sigma-Aldrich). The plates were then incubated for 3 d at 28°C.
The coding regions of the transcription factors were cloned using standard protocols with the Roche Expand High Fidelity PCR system using gene-specific primers (Supplemental Table S1), with appropriate restriction sites incorporated. Transcription factors were then subcloned into pIVEX1.3 WG (Invitrogen) according to the manufacturer's instructions.
In vitro translation of transcription factors was performed using the RTS 100 Wheatgerm CECF kit (Roche) using pIVEX1.3WG-transcription factor constructs. Translations were performed according to the manufacturer's instructions. For each reaction, 900 µL of feeding solution, 80 µL of amino acids, and 20 µL of Met was added to the feeding compartments of the CECF module. To the reaction compartment, 15 µL of reaction mix, 4 µL amino acids, 1 µL Met, 15 µL of wheat germ lysate, 15 µL RNase and DNase free sterile water, and 2 to 4 µg of plasmid DNA were added. The CECF module was loaded into the RTS Proteomaster instrument (Roche) and set to 24°C, shaking at 900 rpm for up to 24 h. Reactions were run on SDS-PAGE gels and detected with anti-His6-tag antibody to identify the translated protein.
EMSAs were performed using the Lightshift Chemilluminescent EMSA kit (Pierce) using biotinylated oligonucleotides (Supplemental Table S1; Sigma-Aldrich). Oligonucleotides were annealed at 95°C for 5 min, with the temperature decreasing by 1°C for each minute and thereafter until holding 4°C. EMSAs were performed according to the manufacturer's instructions with the LightShift Chemiluminescent EMSA kit (Thermo), with final concentrations of 1x binding buffer, 50 ng/µL poly dl-dC, 2.5% (v/v) glycerol, 0.05% (v/v) Nonidet P-40, 5 mM MgCl2, 40 fmol biotinylated oligonucleotides, 1 µg expressed protein, and 4 pmol competitor oligonucleotides, if applicable. Reactions were incubated at room temperature for 20 min before loading onto a 5% native polyacrylamide gel in 0.5x TBE. The gel was electrophoresed for 7 h at 4°C before transferring onto Hybond N+ membrane (GE Healthcare) at 150 mA for 2 h using a semidry blotting apparatus (Millipore). The membrane was fixed with 120 mJ/cm UV-C radiation using a UV-light cross-linker (UVItec). Blocking, washing, and detection were performed using the Chemiluminescent Nucleic Acid Detection Module (Thermo) according to the manufacturer's instructions. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers At3g22370 (AOX1a), At3g24650 (ABI3), and At2g40220 (ABI4).
The following materials are available in the online version of this article.
Received April 9, 2009; accepted May 22, 2009; published May 29, 2009.
1 This work was supported by the Australian Research Council Centre of Excellence in Plant Energy Biology (CEO561495). 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: James Whelan (seamus{at}cyllene.uwa.edu.au).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.139782 * Corresponding author; e-mail seamus{at}cyllene.uwa.edu.au.
Bossi F, Cordoba E, Dupré P, Mendoza MS, Román CS, León P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant J (in press) Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499–1510 Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14: 1–15[CrossRef][Web of Science][Medline] Clifton R, Lister R, Parker KL, Sappl PG, Elhafez D, Millar AH, Day DA, Whelan J (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol Biol 58: 193–212[CrossRef][Web of Science][Medline] Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743[CrossRef][Web of Science][Medline] Comelli RN, Viola IL, Gonzalez DH (2009) Characterization of promoter elements required for expression and induction by sucrose of the Arabidopsis COX5b-1 nuclear gene, encoding the zinc-binding subunit of cytochrome c oxidase. Plant Mol Biol 69: 729–743[CrossRef][Web of Science][Medline] Dekkers BJ, Schuurmans JA, Smeekens SC (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol Biol 67: 151–167[CrossRef][Web of Science][Medline] Dojcinovic D, Krosting J, Harris AJ, Wagner DJ, Rhoads DM (2005) Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Mol Biol 58: 159–175[CrossRef][Web of Science][Medline] Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15: 1212–1226 Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol 89: 1311–1317 Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5: 765–771[CrossRef][Web of Science] Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10: 1043–1054 Finnegan PF, Soole KL, Umbach AL (2004) Alternative mitochondrial electron transport proteins in higher plants. In DA Day, H Millar, J Whelan, eds, Plant Mitochondria: From Genome to Function, Vol 17. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 163–230 Gamborg O (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50: 151–158[CrossRef][Web of Science][Medline] Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 117: 1233–1240 Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan Y-F, Howell K, Ivanova A, Pogson BJ, Millar AH, et al (2008) The absence of Alternative Oxidase 1a in Arabidopsis thaliana results in acute sensitivity to combined light and drought stress. Plant Physiol 147: 595–610 Gutierres S, Sabar M, Lelandais C, Chetrit P, Diolez P, Degand H, Boutry M, Vedel F, de Kouchkovsky Y, De Paepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 94: 3436–3441 Hattori T, Terada T, Hamasuna S (1995) Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7: 913–925[CrossRef][Web of Science][Medline] Ho LHM, Giruad E, Uggalla V, Lister R, Glen A, Thirkettle-Watts D, Van Aken O, Whelan J (2008) Identification of regulatory pathways controlling gene expression of stress responsive mitochondrial components in Arabidopsis. Plant Physiol 147: 1858–1873 Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14: 3271–3284 Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet (in press) Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316: 715–719 Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354: 110–116[CrossRef][Web of Science][Medline] Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine. Genome Res 16: 414–427 Lister R, Chew O, Lee MN, Heazlewood JL, Clifton R, Parker KL, Millar AH, Whelan J (2004) A transcriptomic and proteomic characterization of the Arabidopsis mitochondrial protein import apparatus and its response to mitochondrial dysfunction. Plant Physiol 134: 777–789 Liu Z, Butow RA (1999) A transcriptional switch in the expression of yeast tricarboxylic acid cycle genes in response to a reduction or loss of respiratory function. Mol Cell Biol 19: 6720–6728 Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40: 159–185[CrossRef][Web of Science][Medline] Moore AL, Siedow JN (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059: 121–140[Medline] Narsai R, Howell KA, Millar AH, O'Toole N, Small I, Whelan J (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell 19: 3418–3436 Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14: 2565–2575 Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739–759[CrossRef][Medline] Ooms J, Leon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana (a comparative study using abscisic acid-insensitive abi3 mutants). Plant Physiol 102: 1185–1191[Abstract] Pesaresi P, Masiero S, Eubel H, Braun HP, Bhushan S, Glaser E, Salamini F, Leister D (2006) Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18: 970–991 Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10: 600–606[CrossRef][Web of Science][Medline] Rhoads DM, McIntosh L (1991) Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc Natl Acad Sci USA 88: 2122–2126 Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7: 177–194[CrossRef][Web of Science][Medline] Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6: 471–478[CrossRef][Web of Science][Medline] Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29: 426–434[CrossRef][Medline] Roschzttardtz H, Fuentes I, Vasquez M, Corvalan C, Leon G, Gomez I, Araya A, Holuigue L, Vicente-Carbajosa J, Jordana X (2009) A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis. Plant Physiol 150: 84–95 Söderman E, Mattsson J, Engström P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10: 375–381[CrossRef][Web of Science][Medline] Strodtkötter I, Padmasree K, Dinakar C, Speth B, Niazi PS, Wojtera J, Voss I, Do PH, Nunes-Nesi A, Fernie AR, et al (2009) Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. Mol Plant 2: 284–297 Thirkettle-Watts D, McCabe TC, Clifton R, Moore C, Finnegan PM, Day DA, Whelan J (2003) Analysis of the alternative oxidase promoters from soybean. Plant Physiol 133: 1158–1169 Umbach AL, Wiskich JT, Siedow JN (1994) Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Lett 348: 181–184[CrossRef][Web of Science][Medline] Vanlerberghe GC, McIntosh L (1997) ALTERNATIVE OXIDASE: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48: 703–734[CrossRef][Web of Science] Vidal M, Legrain P (1999) Yeast forward and reverse ‘n’-hybrid systems. Nucleic Acids Res 27: 919–929 Watanabe CK, Hachiya T, Terashima I, Noguchi K (2008) The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant Cell Environ 31: 1190–1202 Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383–395[CrossRef][Web of Science][Medline] Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M, et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302: 842–846 Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48: 606–614 Yoshida K, Watanabe C, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49: 592–603 Zarkovic J, Anderson SL, Rhoads DM (2005) A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis. Plant Mol Biol 57: 871–888[CrossRef][Web of Science][Medline] Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632
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