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Delta subclass HD-Zip proteins and a B-3 AP2/ERF transcription factor interact with promoter elements required for expression of the Arabidopsis cytochrome c oxidase 5b-1 gene

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Abstract

We have identified transcription factors that interact with a promoter region involved in expression of the Arabidopsis thaliana COX5b-1 gene, which encodes an isoform of the cytochrome c oxidase zinc binding subunit. Elements with the core sequence ATCATT, involved in induction by sugars, are recognized both in vitro and in one-hybrid assays in yeast by HD-Zip proteins from the delta subclass and, though less efficiently, by the trihelix transcription factor GT-3b. DistalB-like elements (CCACTTG), required for induction by abscisic acid (ABA), interact with ESE1, a member of the B-3 subgroup of AP2/ERF transcription factors. The HD-Zip protein Athb-21 and ESE1 are able to interact in yeast two-hybrid assays with the ABA responsive element binding factor AREB2/ABF4, which binds to a G-box absolutely required for expression of the COX5b-1 gene. Overexpression of the identified transcription factors in plants produces an increase in COX5b-1 transcript levels. Moreover, these factors are able to induce the expression of a reporter gene located in plants under the control of the relevant COX5b-1 promoter regions required for expression. Analysis of promoter regions of COX5b genes from different plant species suggests that the identified transcription factors were recruited for the regulation of COX5b gene expression at different stages during the evolution of dicot plants.

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References

  • Arce AL, Raineri J, Capella M, Cabello JV, Chan RL (2011) Uncharacterized conserved motifs outside the HD-Zip domain in HD-Zip subfamily I transcription factors; a potential source of functional diversity. BMC Plant Biol 11:42

    Article  PubMed  CAS  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426

    Article  PubMed  CAS  Google Scholar 

  • Ayadi M, Delaporte V, Li YF, Zhou DX (2004) Analysis of GT-3a identifies a distinct subgroup of trihelix DNA-binding transcription factors in Arabidopsis. FEBS Lett 562:147–154

    Article  PubMed  CAS  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    Article  PubMed  CAS  Google Scholar 

  • Busk PK, Pagès M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  PubMed  CAS  Google Scholar 

  • Charrier B, Champion A, Henry Y, Kreis M (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol 130:577–590

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Comelli RN, Gonzalez DH (2009a) Identification of regulatory elements involved in expression and induction by sucrose and UV-B light of the Arabidopsis thaliana COX5b-2 gene, encoding an isoform of cytochrome c oxidase subunit 5b. Physiol Plant 137:213–224

    Article  PubMed  CAS  Google Scholar 

  • Comelli RN, Gonzalez DH (2009b) Divergent regulatory mechanisms in the response of respiratory chain component genes to carbohydrates suggests a model for gene evolution after duplication. Plant Signal Behav 4:1179–1181

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signaling. Protoplasma 245:3–14

    Article  PubMed  CAS  Google Scholar 

  • Elorza A, León G, Gómez I, Mouras A, Holuigue L, Araya A, Jordana X (2004) Nuclear SDH2-1 and SDH2-2 genes, encoding the iron-sulfur subunit of mitochondrial complex II in Arabidopsis, have distinct cell-specific expression patterns and promoter activities. Plant Physiol 136:4072–4087

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes and APETALA2 domain protein. Plant Cell 10:1043–1054

    PubMed  CAS  Google Scholar 

  • Giegé P, Sweetlove LJ, Cognat V, Leaver CJ (2005) Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17:1497–1512

    Article  PubMed  Google Scholar 

  • Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez DH, Welchen E, Attallah CV, Comelli RN, Mufarrege EM (2007) Transcriptional coordination of the biogenesis of the oxidative phosphorylation machinery in plants. Plant J 51:105–116

    Article  PubMed  CAS  Google Scholar 

  • Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139:509–518

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 20:3901–3907

    Google Scholar 

  • Lee WY, Lee D, Chung WI, Kwon CS (2009) Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 58:511–524

    Article  PubMed  CAS  Google Scholar 

  • Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY (2010a) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 153:716–727

    Article  PubMed  CAS  Google Scholar 

  • Lee SJ, Park JH, Lee MH, Yu JH, Kim SY (2010b) Isolation and functional characterization of CE1 binding proteins. BMC Plant Biol 10:277

    Article  PubMed  CAS  Google Scholar 

  • Li JF, Park E, Albrecht G, von Arniml AG, Nebenführ A (2009) The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species. Plant Methods 5:6

    Article  PubMed  Google Scholar 

  • Meijer AH, Ouwekerk PBF, Hoge HC (1998) Vectors for transcription factor cloning and target site identification by means of genetic selection in yeast. Yeast 14:1407–1416

    Article  PubMed  CAS  Google Scholar 

  • Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104

    Article  PubMed  CAS  Google Scholar 

  • Mufarrege EF, Curi GC, Gonzalez DH (2009) Common sets of promoter elements determine the expression characteristics of three Arabidopsis genes encoding isoforms of mitochondrial cytochrome c oxidase subunit 6b. Plant Cell Physiol 50:1393–1399

    Article  PubMed  CAS  Google Scholar 

  • Mufarrege EF, Gonzalez DH, Curi GC (2011) Functional interconnections of Arabidopsis exon junction complex proteins and genes at multiple steps of gene expression. J Exp Bot 62:5025–5036

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  PubMed  CAS  Google Scholar 

  • Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575

    Article  PubMed  CAS  Google Scholar 

  • Palena CM, Gonzalez DH, Guelman S, Chan RL (1998) Expression of sunflower homeodomain containing proteins in Escherichia coli: purification and functional studies. Protein Expression Purif 13:97–103

    Article  CAS  Google Scholar 

  • Park HC, Kim ML, Kang YH et al (2004) Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135:2150–2161

    Article  PubMed  CAS  Google Scholar 

  • Reynolds A, Lundblad V, Dorris D, Keavency M (1997) Yeast vectors and assays for expression of cloned genes. In: Ausubel F, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Green Publishing and Wiley-Interscience, New York, pp 13.6.1–13.6.6

  • 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

    Article  CAS  Google Scholar 

  • Sedmak J, Grossberg S (1977) A rapid, sensitive, and versatile assay for protein using Coomassie Brilliant Blue G-250. Anal Biochem 79:544–552

    Article  PubMed  CAS  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    PubMed  CAS  Google Scholar 

  • Shen QJ, Casaretto JA, Zhang P, Ho THD (2004) Functional definition of ABA-response complexes: the promoter units necessary and sufficient for ABA induction of gene expression in barley (Hordeum vulgare L.). Plant Mol Biol 54:111–124

    Article  PubMed  CAS  Google Scholar 

  • Smith DB, Johnson KS (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31–40

    Article  PubMed  CAS  Google Scholar 

  • Söderman EM, Broccard IM, Lynch TJ, Finkelstein RR (2000) Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol 124:1752–1765

    Article  PubMed  Google Scholar 

  • Tron AE, Comelli RN, Gonzalez DH (2005) Structure of homeodomain-leucine zipper/DNA complexes studied using hydroxyl radical cleavage of DNA and methylation interference. Biochemistry 44:16796–16803

    Article  PubMed  CAS  Google Scholar 

  • Welchen E, Gonzalez DH (2005) Differential expression of the Arabidopsis cytochrome c genes Cytc-1 and Cytc-2: evidence for the involvement of TCP-domain protein binding elements in anther- and meristem-specific expression of the Cytc-1 gene. Plant Physiol 139:88–100

    Article  PubMed  CAS  Google Scholar 

  • Welchen E, Gonzalez DH (2006) Overrepresentation of elements recognized by TCP-domain transcription factors in the upstream regions of nuclear genes encoding components of the mitochondrial oxidative phosphorylation machinery. Plant Physiol 141:540–545

    Article  PubMed  CAS  Google Scholar 

  • Welchen E, Chan RL, Gonzalez DH (2002) Metabolic regulation of genes encoding cytochrome c and cytochrome c oxidase subunit Vb in Arabidopsis. Plant, Cell Environ 25:1605–1615

    Article  CAS  Google Scholar 

  • Welchen E, Chan RL, Gonzalez DH (2004) The promoter of the Arabidopsis nuclear gene COX5b-1, encoding subunit 5b of the mitochondrial cytochrome c oxidase, directs tissue-specific expression by a combination of positive and negative regulatory elements. J Exp Bot 55:1997–2004

    Article  PubMed  CAS  Google Scholar 

  • Welchen E, Viola IL, Kim HJ, Prendes LP, Comelli RN, Hong JC, Gonzalez DH (2009) A segment containing a G-box and an ACGT motif confers differential expression characteristics and responses to the Arabidopsis Cytc-2 gene, encoding an isoform of cytochrome c. J Exp Bot 60:829–845

    Article  PubMed  CAS  Google Scholar 

  • Zabaleta E, Heiser V, Grohmann L, Brennicke A (1998) Promoters of nuclear-encoded respiratory chain complex I genes from Arabidopsis thaliana contain a region essential for anther/pollen-specific expression. Plant J 15:49–59

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Li Z, Quan R, Li G, Wang R, Hyang R (2011) An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol 157:854–865

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from ANPCyT (Agencia Nacional de Promoción Científica y Tecnológica, Argentina). RNC was a fellow of ANPCyT; EW and DHG are members of CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina). JCH was supported by the Basic Research Program (#2010-0012801) of the National Research Foundation (NRF) funded by MOEST and the Next-Generation BioGreen 21 Program (#PJ008173), RDA, Republic of Korea.

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Authors and Affiliations

  1. Instituto de Agrobiotecnología del Litoral (CONICET-UNL), Cátedra de Biología Celular y Molecular, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, CC 242 Paraje El Pozo, 3000, Santa Fe, Argentina

    Raúl N. Comelli, Elina Welchen & Daniel H. Gonzalez

  2. Division of Applied Life Sciences (BK21 Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 660-701, Korea

    Hye Jin Kim & Jong Chan Hong

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  1. Raúl N. Comelli
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  2. Elina Welchen
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  4. Jong Chan Hong
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  5. Daniel H. Gonzalez
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Correspondence to Daniel H. Gonzalez.

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Comelli, R.N., Welchen, E., Kim, H.J. et al. Delta subclass HD-Zip proteins and a B-3 AP2/ERF transcription factor interact with promoter elements required for expression of the Arabidopsis cytochrome c oxidase 5b-1 gene. Plant Mol Biol 80, 157–167 (2012). https://doi.org/10.1007/s11103-012-9935-9

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